Identifying the barriers to universal cervical length screening for preterm birth prevention at a tertiary hospital in Thailand (patient’s perspectives): implementation research

To identify patient perspectives of barriers to cervical length screening to prevent preterm births. In Phase I of this prospective descriptive implementation study, 40 pregnant women of up to 24 week gestation were interviewed. Phase II comprised questionnaire development and data validation. The questionnaire was subsequently administered to 400 participants in Phase III. Most participants (74.3%) realised preterm babies have complications and high care costs (53%). They recognised that premature-birth risk identification enables appropriate pregnancy care (93.8%), but they were unaware that cervical length measurements indicate the risk (59.5%). The participants who were aware wanted to be examined (63.5%) because of concern about preterm birth (95.8%). Husbands were reported to influence decision-making about screening (81.3%) and subsequent treatment (42.5%). If the associated costs were subsidised, the majority of participants (67.3%) would undergo screening. Physicians do not explain ways to prevent preterm births. Government policy on preventing preterm births is not well established. Screening and treatment costs are major barriers. Thai Clinical Trials Registry (TCTR) number: TCTR20190813003


Introduction
A preterm birth, which is one occurring before 37 weeks of gestation [1] is associated with many adverse neonatal outcomes, including respiratory problems, intraventricular haemorrhage, visual problems, seizures and long-term neurological disorders [2,3]. In Thailand, there are an estimated 15,000 cases of preterm births annually [4]. Expenditure on preterm neonatal hospital care has been calculated to be in the order of 170,000 Baht/case (US $5300/case), which equates to a total of 255,000,000 Baht/year (US $79,680,000/year). These figures exclude the long-term care costs incurred following hospital discharge [4].
Progesterone supplementation is used to prevent preterm births in pregnant women with a short cervix or with a history of preterm deliveries. This steroid hormone plays an important role in parturition [5]. Research has found that progesterone levels reduce considerably as the process of labour progresses. The hormone has, therefore, been recently The original online version of this article was revised due to correction in the name of the 3rd author. used to prevent preterm labour and to enhance the effects of other drugs to inhibit uterine contractions [5]. The use of cervical cerclage and pessaries also appear to have similar effectiveness as management strategies for preterm birth prevention in women with singleton pregnancy, a previous spontaneous preterm birth, or a short cervix [6].
Sixty percent of preterm births are idiopathic [7]. Pregnant women with a history of preterm births represent only 7% of women with premature deliveries [8]. There is a higher risk of a preterm birth among women who have a short cervix (< 25 mm) between 18 and 24 weeks of gestation [9,10]. A short cervix is believed to be caused by a decrease in progesterone, resulting in a weakening of the mucus in the cervix (the mucus plug). The mucus plug imparts anti-infective properties to the cervix [11,12], and the anti-inflammatory properties of chorion and amnion result in a short cervix [13,14], leading to the most common pathway to premature delivery. However, a cervix is not always short due to low progesterone levels; other causes include genetic factors, trauma, abnormalities of the cervix or uterus, or cervical insufficiency (also termed incompetent cervix) [15].
The need to use progesterone supplementation implies that pregnant women with a history of preterm labour do not have sufficient levels of the hormone to prevent premature delivery. There is also an elevated risk of preterm births among pregnant women with a short cervix, and this condition is the most common reason for premature deliveries. Universal cervical length screening is, therefore, imperative for all pregnant women [14][15][16][17].
Although the use of cervical length measurement to detect women with an elevated risk of preterm labour has been advocated for many years, there are obstacles to its widespread adoption. The objective of this research was to identify the barriers to cervical length screening from the perspectives of pregnant women.

Materials and methods
This was a prospective, descriptive, implementation study. Before its commencement, it was approved by the Siriraj Ethics Committee of the Faculty of Medicine Siriraj Hospital (Si 343/2562) and registered at the Thai Clinical Trials Registry (TCTR20190813003). We thank the Faculty of Medicine Siriraj Hospital, Mahidol University for its funding support [(IO) R016233023].
This survey study utilised questionnaires. To ensure an adequately sized dataset, with a proportion of the results of interest of 50% (p = 0.5), an estimation error of ≤ 5% and a 95% confidence level (type I error = 0.05, 2-sided), the number of pregnant women needing to be surveyed was calculated to be ≥ 385.

Phase I: in-depth interviews
This phase collected information on 7 areas: (1) general information on participants; (2) attitudes towards preterm birth; (3) attitudes towards prenatal cervical length measurement; (4) attitudes towards prevention of preterm birth; (5) attitudes towards the method of prevention of preterm birth; (6) decision-making relating to undergoing cervical length measurement; and (7) decision-making relating to engaging in preterm-birth prevention after the detection of a short cervix.
The in-depth interviews were conducted on 40 pregnant women of up to 24 week gestation who had been recruited for the study. Prior to the interviews, these women had expressed a willingness to participate in the research project and had been invited to a private counselling room. After the details of the project were described, the women were given time to ask questions and to consider whether they wished to formally enrol in the trial. The women were advised that they could decline to participate or could withdraw at any stage if they so desired. Those women who decided to volunteer as a research subject were asked to sign an informed consent form before being interviewed at length.
The participants were asked for permission for the conversations and the structured interview to be audio recorded. The subjects initially completed an attitude assessment questionnaire, which focussed on cervical length assessment and the risk of a preterm birth. Several other aspects were then investigated in a structured interview. One related to the frustration felt during any prior decision that may have been made to request a cervical length measurement and the subsequent performance of that procedure. There was also an assessment of any grievances related to any prior request for a cervical length measurement, and about a decision to undergo preterm birth prevention if a short cervix had been detected. The total time from the commencement of the questionnaire until the completion of the comprehensive interview was about 30 min. The data integrity of the research questions was later verified.

Phase II: development and validation of questionnaire
The data obtained from the questionnaire and in-depth interviews were analysed to determine the means and standard deviations. This enabled the questionnaire and interview questions to be refined. The revised questionnaires and interview questions were tested for validity and reliability before being used in the third and last phase.

Phase III: administration of questionnaire
The validated questionnaires were given to 400 patients in the antenatal ward of the hospital during the final phase of the study.

Statistical analysis
Demographic data were summarised using descriptive statistics. Categorical data are presented as numbers and percentages, while continuous data are presented as mean ± standard deviation or median and range. The statistical analyses were performed using PASW Statistics for Windows (version 18.0; SPSS Inc., Chicago, Ill., USA). Attitudes towards prenatal cervical length measurement are detailed in Table 3. Nearly all of the women accepted that screening to determine the risk of premature birth is useful, because it permits the undertaking of planning for appropriate care during the pregnancy [375/400 (93.8%)]. However, over half had no knowledge about the use of cervical length measurement to predict preterm deliveries [238/400 (59.5%)]. Most of the participants believed that methods are available to prevent preterm birth [269/400 (67.3%)], and they reported that they were prepared to immediately undergo an assessment of risk [293/400 (73.2%)]. Multiple responses were permitted for the questions relating to attitudes to the method of prevention of preterm birth (Table 4). Three quarters of the participants expressed concern about experiencing pain during a trans-vaginal examination [277/400 (69.3%)]. In addition, half indicated that they were unaware of alternative methods to prevent preterm birth [194/400 (48.5%)].

General information on the participants is presented in
Multiple responses were also allowed for the questions relating to deciding whether to undergo the cervical length measurement procedure (Tables 5, 6). The main reason for refusing an examination was concern about the possibility of a miscarriage [189/400 (47.3%)]. If a short cervix were found and treatment were recommended, three quarters of the participants indicated that they would accept every  Table 7 itemises grievances related to participant decisions to undergo preterm birth prevention after the detection of a short cervix. Most participants had never been advised by a physician to consider undergoing a cervical length measurement procedure to prevent a preterm birth [266/400 (66.5%)]. Two thirds indicated that they would immediately agree to a cervical length measurement if their healthcare provider supported the cost of treatment [269/400 (67.3%)].

Discussion
Our data revealed that most of the surveyed women had positive attitudes towards preterm birth prevention. They believed that there were methods available to prevent preterm births, and they expressed a willingness to immediately utilise a preventive method. On the other hand, the results of our research also indicated that not only did most of the women not know how to prevent a preterm birth, but they were unaware of the cervical-length-measurement screening method. Even though they knew that premature infants suffer from many complications and that their costs of care are high, few of the pregnant women had been assessed for their risk of a preterm birth via cervical length screening. Our research also found that most of the pregnant women did not know that the Ministry of Health, Thailand, has a policy of preventing preterm births through the performance of cervical length measurement screening [307/400 (76.8%)]. In addition, the women indicated that they would need financial support from the Ministry of Health to meet the costs of screening and further medical treatment if an elevated risk of a preterm birth were identified.
Cervical length screening is the established preterm birth screening method and is applied to singleton pregnancies during the second trimester [16]. Although pregnant women with a history of preterm deliveries have a four-to sixfold greater risk of having a preterm delivery than women without such a history, preterm births are most common with first pregnancies [17]. Therefore, universal cervical length It is not a problem or difficult, because it is just a small child born prematurely 106 (26.5%) It is a problem and difficult, because there is no-one to provide support 2 (0.5%) It is a problem and difficult, because the child has many complications and the cost of care for the child is very high 212 (53.0%) Not sure 80 (20%) Opinion as to whether a premature birth harms their life and their family There is no problem or harm in any way 132 (33.0%) Life seems to be more difficult because of having to take care of a premature baby 143 (35.8%) Not sure 125 (31.3%) If unborn baby is at risk of preterm birth, they will find a way to prevent it There is no need to take defensive measures, because they are confident that they have no risk 21 (5.3%) They must find a way to prevent the preterm birth, because they don't want the baby to be born prematurely 344 ( 1 3 measurement screening is necessary; it is one of many methods available for screening for pregnant women at risk of preterm delivery. Women with a positive screening result of a short cervix are treated with progesterone. The use of this hormone has proven to be effective in preventing preterm births [18]. and it reduces the mortality and disability rates of preterm neonates. The cost of providing care for premature babies is, therefore indirectly reduced through the administration of progesterone. Unfortunately, pregnant women receiving antenatal care rarely have their cervical lengths measured even though the use of this technique can prevent premature births. Our research found that 93.2% of our study cohort were having their first pregnancy. Most of the women were aware that preterm babies have a high morbidity, require extensive care, and need different treatment from full-term babies. They also knew that the cost of care for these infants is high due to the substantial number of possible complications. On the other hand, the vast majority did not know that a cervical length measurement can help to identify women at risk of a preterm delivery, thereby allowing appropriate treatment to be initiated to prevent a preterm birth [314/400 (78.5%)]. Had they known earlier, the large majority stated that they would have immediately requested a screening test (73.2%).
Most of the pregnant women did not know how cervical length is actually measured [302/400 (75.5%)]. Specifically, they were unaware that the vaginal-ultrasound method requires the insertion of a probe into the vagina. After hearing a description of the methodology, two thirds expressed concern about having a miscarriage [271/400 (67.8%)]. All of their anxiety would be eased if a doctor described the benefits of the technique and how it is used to screen for the risk of a preterm birth. It was also found that the vast majority of the women receiving antenatal care were having their first pregnancy. Although most knew that measuring the cervical length could be used as part of the process of preventing premature births, very few had had the procedure. Most knew that the treatment and levels of care of preterm babies are different to those of full-term babies, and that the cost of care for preterm infants can be extremely high because of the numerous potential medical complications. By contrast, the vast majority did not know that having a cervical length measurement can help to prevent preterm births [314/400 (78.5%)]. If the method were known to be important, 73.2% of the pregnant women stated that they would immediately request a screening test, even though most did not know the measurement methodology [302/400 (75.5%)]. Having doctors routinely advising pregnant women about the benefits and methods of the test would be of great benefit and would indirectly help to prevent preterm births.
Although cervical length measurement is the standard method for the prevention of preterm births [19], most physicians do not recommend it. If physicians do not consider the possibility of a preterm delivery, they will not utilise the methods available for its prevention, screening and treatment, thereby resulting in a reduction of the use of the cervical-length-measurement screening method [20]. Moreover, if physicians hold the view that such screening is not helpful, pregnant women will not be given a screening test, placing them at risk of having a preterm birth. Moreover, physicians who have never previously encountered a preterm birth may not advise pregnant women under their care to have cervical length measurement screening [21].
To achieve the goal of providing universal cervical length measurement screening, pregnant women could be counselled on the prevention of a preterm birth through a cervical length measurement using pictures, pamphlets, or video guides. The provision of patient education based

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on such visual material would facilitate understanding by pregnant women and thereby aid their decision-making on whether to undergo cervical length measurement screening [22]. Moreover, as our research found that the husbands of pregnant women have by far the biggest influence on that decision-making process, information on the screening process should be provided to couples. If the pregnant women were found to have a positive screening test result (a short cervix, or at risk of a preterm birth), 69.8% of them reported that would request interventions to prevent a preterm birth irrespective of the associated costs. If the costs were a problem, a third of the women stated that would still make every effort to have those interventions [125/400 (31.3%)]; however, a slightly smaller proportion believed that they would be unable to do so [108/400 (27.0%)]. As their husbands (42.5%) would influence the decision as to whether to proceed with action to prevent a preterm birth, couples should be counselled together on screening and treatment planning. However, if the cost of screening and treatment were supported by the government, two thirds of the pregnant women indicated that they would decide to undergo those procedures without first seeking the opinion of their husbands [269/400 (67.3%)]; this suggests that the current screening and treatment costs are a significant barrier to uptake. Consideration should, therefore, be given to conducting a cost-effectiveness analysis of progesterone treatment and preterm care that are financially supported by the government.
Temming et al. [23] found that cervical length measurements tended to be rejected by women with one or more of the following characteristics: African, American, or Hispanic; obese; multiparous; younger than age 35; and a smoker. Their research also revealed that the rate of early spontaneous preterm births was higher among those women than other groups. In addition, the researchers established that the incidence of pregnant women with a cervical length of ≤ 20 mm was 1.1%, with no significant differences in the preterm delivery rates of women who underwent, and those who did not undergo, the measurements [23]. Pedretti and colleagues [24] also found that there are a number of barriers that may prevent the implementation of a universal cervical length screening program. They include cost, availability of vaginal progesterone and other treatment options, and the reluctance of women to undergo transvaginal ultrasound. All of those factors are consistent with the findings of our study.
In summary, from the perspectives of patients, there are several barriers to undergoing cervical length measurement screening. Firstly, physicians generally do not explain that there are ways to prevent preterm births, and the methods available to measure the length of a cervix are typically not clarified to patients. Moreover, pregnant women tend to be anxious about the possibility of having a miscarriage; their concern could be allayed through the provision of appropriate physician counselling. In addition, the government's policy on preventing preterm births has not yet been well established among clinicians. The costs of the screening test and treatment after a positive test result are also a problem for an appreciable proportion of pregnant women. Most stated that they want the government to provide financial support for the provision of the screening and treatment. Finally, husbands have the most influence on patients' decision-making as to whether to proceed with screening and treatment to prevent a preterm birth.

Conclusions
From patient's perspectives, there are two main barriers to their uptake of universal cervical length screening for preterm birth prevention. One is a lack of knowledge of the benefits of the screening test; the other is unclear Ministry of Health policies relating to the prevention of preterm births. Pregnant women would be likely to undertake cervical length screening for preterm birth prevention if appropriate information were provided and the costs of the screening test and treatment in high-risk cases were subsidised. The use of progesterone drugs or a cervical suture to reduce the risk of a preterm birth in high-risk cases should be considered.