Googling preterm prelabour rupture of the membranes: A systematic review of patient information available on the internet

Preterm prelabour rupture of the membranes (PPROM) complicates 3% of pregnancies and is associated with an increased risk of maternal and perinatal morbidity and mortality. In an attempt to better understand this diagnosis, patients routinely resort to the internet for medical information. The lack of governance online leaves patients at risk of relying on low‐quality websites.

prolapse and placental abruption. 2 Poor maternal and perinatal outcomes are inversely associated with gestational age at PPROM; and there is a recognised association between PPROM and adverse maternal mental health outcomes. Although there is clinical guidance regarding this diagnosis, there is variation in the language used to describe the condition as well as management. 1,3 Google alone sees around 3.5 billion searches per day, 4 with an estimated 4.5-15% being health-related queries. 5,6 Seventy-one percent of women report using Google to obtain healthcare information, second only in popularity to family and friends (74%). Meanwhile, 84% report not feeling listened to by their healthcare professional, and only 59% use them as a source of healthcare information. 7 Although the internet provides an opportunity for dissemination of easy-to-access information for patients, there is no quality assurance online. 8 This results in patients being left to determine the quality of information themselves, which most find challenging, 9 and results in frustration associated with searches. 10 In conditions such as PPROM, where decision-making is often complex, high-quality information that is easy to understand is likely to improve patients' ability to participate in decision-making and reduce anxiety. Systematic reviews of search engines have previously been used to assess available patient information in gynaecology [11][12][13] and further afield, for example in neurology. 14 The objective of this study was to assess systematically the accuracy, quality, readability and credibility of English language World Wide Web pages offering information on PPROM.

| M ET HODS
The review was undertaken in line with the Preferred Reporting Instrument for Systematic Review and Metaanalysis (Table S1).

| Search strategy
A search strategy was developed in consultation with patients who advised on searches they were most likely to run regarding PPROM (Table 1). During June 2022 the five most popular English language search engines were searched: Google, Bing, Yahoo, Ask and AOL. Location services were disabled, and browser history was deleted before and between searches to reduce bias. The first page of results, including sites paying for advertising, were considered for inclusion in all cases because people rarely look beyond this when carrying out searches. 15 Pages found from search engines were included where they provided at least 300 words of health information related to PPROM on the first page clicked through from the search engine, or when clicking on an obvious 'about' page where the search engine takes the searcher to a home page.
Exclusion criteria were: (1) non-English sites; (2) those aimed at professionals (e.g. clinical guidelines and scientific papers); (3) inaccessible (for example, because of password protection); (4) contents exclusively relating to individual's experience (such as a blog); (5) excessive advertising (more than two advertisements per page); and (6) pages discussing other diagnoses or topics, including term rupture of membranes.
Two reviewers (MH and LS) screened the full pages of all potentially eligible web pages. Any discrepancies were discussed with a third reviewer (AS) and agreed upon.

| Data extraction
In the absence of a core outcome set for healthcare information, outcomes measured were based on similar studies; 11-13 the priorities of our patient involvement group, and the priorities of healthcare professionals working within the field as determined by a survey of both groups.
A data extraction protocol was developed and piloted on a representative sample of web pages before data extraction from all included web pages. Data were extracted by two reviewers (MH and LS) with discrepancies discussed. Any remaining uncertainties were resolved by a third reviewer (AS). Authors who had been involved in writing any pages reviewed were not invited to comment on those pages. Basic data extracted from all web pages included country of origin, listed authors, provision of any references and privacy statements.
Readability was determined using the Flesch-Kincaird Scale. 16 This reports a score from up to 100 (where 100 is the least complex) for any given body of text using the formula 206.835-10.15 (total words/total sentences)−84.6 (total words/total syllables). These scores can then be converted into estimated reading ages. In the UK, 56% of the population have a reading age equivalent to 7 years or more, 17 although recommended reading age is 9-11 years for healthcare information, and not to exceed 14 years. 18 Therefore, we considered reading age equivalent to 11 years to be suitable for online information.
Credibility was assessed using the White criteria, which are validated for assessment of health information. 19 They give a score from 0 to 9 with higher scores meaning greater credibility. We determined scores of 7 or more to indicate a reliable source in line with previous similar work. 13 We assessed material from regions where health care is paid for at source to ensure that the material was not primarily advertising a particular treatment facility.  Quality was assessed using the DISCERN scale, which is validated to assess the quality of written health information, and give a score from 0 to 85. 20 As per similar publications, we assessed a score of 53 or greater to reflect high-quality information; 28-52 moderate-quality information; and 27 or less low-quality information. 13

| Development of accuracy scoring
Accuracy scoring was based on the Royal College of Obstetricians and Gynaecologists (RCOG) Green Top Guideline Number 73 Care of Women Presenting with Suspected Preterm Prelabour Rupture of Membranes from 24 +0 Weeks of Gestation. 1 This guideline was chosen because of its recent publication, international use and free accessibility online to both healthcare providers and the public. In order to determine which parts of the guideline ought to be scrutinised, its recommendations were sent to a group of relevant healthcare professionals (obstetricians, midwives and neonatologists) and also (in plain English) to patients who had previously experienced PPROM. Four statements were modified for ease of understanding: two statements advising steroids from 24 +0 to 25 +6 , and also 26 +0 and 33 +6 weeks of gestation were combined into a single statement; and two statements advising considerations for continuing pregnancy until 37 +0 weeks of gestation, and timing of delivery for group B streptococcus-positive patients were combined into a single statement. The recommendations were followed by one statement that read 'There is no national guidance on the management of PPROM at <24 weeks of gestation' included at the suggestion of our patient involvement group. All participants were asked to score each recommendation in terms of relevance to care. A list of recommendations endorsed by each group was formulated to assess accuracy. Pages were scored 2 if they included accurate information on the topic; one for partially accurate information; and 0 for missing or inaccurate information. This generated a maximum score of 22. This approach has been used in other similar work. 13 Note was made of pages referring to specific outcomes arising from PPROM: maternal sepsis, iatrogenic preterm delivery secondary to chorioamnionitis, poorer neonatal outcomes secondary to chorioamnionitis, cord prolapse, placental abruption, and increased risk of perinatal mortality (reference only to increased risk of perinatal mortality where PPROM occurred at less than 24 weeks of gestation was not considered sufficient). Finally, any information that went against the consensus of reasonable scientific or clinical understanding of PPROM was noted.

| Analysis
Characteristics were tabulated and presented with descriptive statistics and supporting figures.

| Patient involvement
Patients were involved at all stages of the study from conception to write up.

| Accuracy scoring
Seventeen healthcare professionals (obstetricians, midwives and neonatologists) and 20 women who had previously experienced PPROM completed the questionnaire. Results for both groups are displayed in Table S2. The top ten concerns for both groups were included in accuracy scoring, giving a maximum score of 22.

| Web page selection process
The website selection process is summarised in Figure 1. All websites identified were English language. After removal of duplicates, 323 websites were identified for screening, and 39 websites were included in the review.

| Web page characteristics
Website characteristics and outcomes are listed in Table S3. Of the 39 websites included, 19 were British in origin, 14 from the USA, and all from high-income, predominantly Englishspeaking countries. Eleven websites gave named authorship, and 21 included at least one reference. Several websites made reference to the same texts (highlighted in Table S2) resulting in 31 different sources for analysis.

| Readability
Readability is summarised in Table 2. The median Flesch-Kincaird score was 57.4 (interquartile range 47.75-64.9), equivalent to a reading age of a 15-to 18-year-old. No websites had a reading age of 11 years or under; 23% were of university-level equivalent.

| Credibility
Median credibility was 4/9 with no websites scoring 7 or above. While 11 sources gave authorship, only nine gave the credentials of their authors, with two reporting their conflicts of interest. Sixteen had evidence of an editorial process, but none reported potential sources of bias. In three cases it was unclear whether the primary purpose of the website was advertising. However, all websites provided some relevant information, with 26 providing practical advice. Twenty-six websites gave date of publication.

| Quality
Three sources gave high-quality information: The RCOG Patient Information Leaflet (2019), When your waters break early; The St Helens and Knowsley Teaching Hospital NHS Trust Patient Information Leaflet Preterm prelabour rupture of membranes (when your waters break early), (which makes reference to, and is substantively based on, the RCOG 2019 patient information leaflet); and the Tommy's page Waters breaking early (PPROM). Of the remaining pages, 24 were of moderate quality and four were of low quality.
There were particularly stark differences in terms of discussion of treatment: while 25 pages gave some description of the purpose of specific treatments, and 29 discussed the benefits of treatments, only three discussed any risks associated with treatment options, and only four pages alluded to women having the option to decline treatment options. Furthermore, only 14 pages made any reference to there being any uncertainty surrounding the diagnosis or management of PPROM. Only ten pages gave signposting to places providing emotional support for women with PPROM.

| Accuracy
Median accuracy score was 9/22 (interquartile range 7-12.5). Of note, there was little relationship between what websites discussed and what women reported to be their main concerns (Table 3) -for example, women reported their top concern to be an opportunity to speak with neonatologists during the antenatal period, but only seven websites fully explained this and 22 did not discuss it at all.
Reference made to emergencies and severe morbidity associated with PPROM is summarised in Table 4. The most discussed emergency was maternal sepsis, with 25 websites discussing this. Only four websites made reference to poorer outcomes in neonates affected by chorioamnionitis compared with those not affected. Two websites discussed all outcomes More often, information was incomplete rather than incorrect, there was only one instance of a website providing information contrary to standard scientific and clinical understanding of PPROM: this website heavily promoted specific diet for 'strengthening of connective tissue' as an intervention women should make.

| Main findings
None of the websites assessed in this study provided highquality, accurate and credible patient information on PPROM. Where websites were high quality, their accessibility to patients was limited by an assumption of reading abilities far above the UK average, or that which is expected of patient information. Common emergencies were not routinely explained. In no case was it made clear to women that they had an option to decline treatment. The information our patient involvement group considered pertinent was not reflected in the information given by websites; this was true even of high-quality, high-accuracy websites, such as the RCOG patient leaflet, although this particular source did make reference to having used their own patient advisory group. There was minimal emphasis on emotional wellbeing (despite this being the third most important priority for patients), with a minority of websites discussing it or providing signposting to further support.

| Strengths and limitations
To our knowledge, this is the first study to assess the accuracy, credibility, readability and quality of information regarding PPROM available online and aimed at patients; and is also the first regarding any obstetric condition. Searches were undertaken systematically across five search engines and validated assessment tools were used. Patients were involved throughout this study. The opinions of patients and relevant healthcare professionals formed the basis of accuracy assessment, so increasing the likelihood that these results reflect how helpful patients truly find information.
There are several limitations to this study. Although only 1% of search results after the first page are read, limiting to the first page of results may have resulted in inadvertent T A B L E 3 Frequency of websites addressing patient involvement groups' priorities.
Patient concern (listed greatest to least)

Number of websites providing no explanation (n = 31), n (%)
Opportunity to discuss care with neonatologists antenatally exclusion of some relevant pages. As no non-English sites were identified, running searches in English probably limits the international applicability of the findings. Our survey had a small sample size, which may not reflect the primary concerns of all women with PPROM, although we could find no published larger sample size. There are few systematic reviews of internet sources, limiting the precedent on which we could base our methods. The lack of international consensus on the management of PPROM means that a national guideline was used to decide what was considered relevant information. This does mean that in some instances the information given within the websites may be relevant to patients in other countries -this was most notable as regards the discrepancy in timing of delivery advice in RCOG versus American College of Obstetricians and Gynecologists guidance. In any instance, use of a UK guideline carries the additional issue that interventions are all subject to National Institute for Health and Care Excellence cost-effectiveness analysis, which may result in different clinical guidance for economic reasons (although we do not believe this is a primary issue in the case of PPROM). The guideline used as a standard is relatively recent (published in 2019): many sites were out of date (for example three gave access to an archived patient information leaflet from RCOG) but were still easily accessible, so likely to cause confusion. One overcame this issue by linking to the RCOG website to ensure information was kept more up-to-date.

| Interpretation
Healthcare professionals must acknowledge that women rely on the internet as a form of healthcare information, often over and above reliance on healthcare professionals. The recently published Women's Health Strategy for England recognises that women need trustworthy and easy-to-understand information regarding their health and have included this in their 10-year strategy's Six Point Plan. 7 We have demonstrated here that, in the case of PPROM, available information is often inaccurate and of low quality.
A lack of publication dates renders it impossible for women to know whether advice is current. There is a failure to highlight biases, conflicts of interest and areas of uncertainty among professionals. Often poor readability reduces the value of published material and serves to further isolate already disenfranchised groups who may have more basic language skills, and ultimately could be a contributing factor to disparate health outcomes. Combined with pre-existing evidence that patients often find it difficult to determine the credibility of information online, this all points towards insufficient opportunity for patients to assimilate relevant knowledge to make informed decisions. Similar findings have been reported in gynaecological conditions, suggesting that this is a more widespread issue in women's health. [11][12][13] Even among higher-scoring sources in our study, contradictory international guidance (and a failure to highlight this) could affect trust in the healthcare system. The absence of information advising women of the risks of treatment, and that they can decide against treatments in part or entirely, reduces their autonomy. All of this amounts to an increased risk of harm, as highlighted by The US Office for Disease Prevention and Health Promotion, that reports a three-part concern regarding inaccurate healthcare online: physical risk, emotional risk and financial risk. 21 PPROM brings particular challenges in terms of information for patients, in particular the balance of maternal and fetal risks in infection, and the potential benefits of preterm delivery over prolonged latency among women in whom chorioamnionitis is suspected. The lack of high-quality information is likely to lead to miscommunication with healthcare teams and introduces the potential for distrust. Furthermore, it disempowers patients who are left less able to make informed and balanced decisions.

| Recommendations for practice: Patient information
This study emphasises that in an attempt to understand a serious complication of pregnancy, women are often faced with inaccurate information. Healthcare professionals must recognise the changing landscape regarding patient information: recent evidence demonstrates that women are more likely to seek healthcare information online than they are from a healthcare professional (71% versus 59%). 7 Although we should continue to strive for online information co-existing alongside personalised conversations between professionals and patients, we must also take responsibility for and prioritise high-quality online information. Although there is a lack of governance regarding what is published online, healthcare professionals bear significant responsibility to ensure patients have access to high-quality information, knowing that the internet does not help women to discern high-quality from low-quality search results. This can be done by individuals, but a uniform strategy throughout the National Health Service (or equivalent structures) would create parity in access as well as improving T A B L E 4 Frequency of reference to emergencies and severe morbidities associated with preterm prelabour rupture of membranes. Increased risk of perinatal mortality 10 (32) quality of information given, and this should be considered an area for prioritisation. Healthcare professionals should also be open to discussing any information that patients have already found. First, sites run by healthcare professionals or medical associations should abide by basic conventions that allow patients to evaluate reliability, such as listing authors and their conflicts of interest. They should also place emphasis on areas of uncertainty and bias, both of which non-expert readers would struggle to determine without significant background knowledge. Even brief discussion of these issues acts as an opportunity to promote interaction with healthcare professionals. Patient groups should be involved at all stages of information design, including decisions regarding pertinent information for inclusion.
There are obvious challenges surrounding simplifying complex health topics to meet reading age requirements, and even high-quality web pages struggled to meet these. Where this issue persists, other modalities must be considered (such as video, audio or infographic). Local and regional healthcare providers should collaborate with their populations to determine the most effective means of communication. Translation into other languages should be considered: where this is costly for smaller organisations then priority should be given to the needs of the local population, and funding should be prioritised. As well as signposting to high-quality information (for example by linking it to online maternity notes, or giving copies out to patients), healthcare professionals must take responsibility for educating patients on the risks of low-quality information, as well as providing strategies to determine how reliable sources are. Although newer initiatives, such as that of the UK Government to prioritise high-quality women's health teaching to school children should be applauded, the majority of patients will not have benefited from these, so pre-existing knowledge should not be assumed. Healthcare professionals must also consider how research is discussed with patients, given that this is often available at least in part, online, and is unlikely to be reflected in formal patient information leaflets. Healthcare professionals must be equipped to help patients understand the implications of research that goes beyond, is contradictory to, or is more recent than guidelines.

| Recommendations for practice: PPROM
Particular complexities of PPROM must be considered, especially surrounding timing of delivery, balancing maternal and fetal risks, and lack of evidence regarding periviability PPROM. Access to high-quality written information regarding these issues would give patients significantly more opportunity to digest information, which could aid their decision-making. This would result in a more collaborative decision-making process, which could have positive implications for patients' mental, as well as physical, health.
Information must also consider the wider-reaching implications of the condition, such as its increased association with antenatal anxiety and postnatal depression, and signpost to support for this. 22,23 Given the often stigmatised nature of mental health, increased awareness of these associations may empower women to ask for help sooner. Early access to additional information on prematurity would also be valuable, especially given the high and enduring rates of anxiety and post-traumatic stress among parents who have had babies cared for on neonatal units. 24

| Recommendations for research
Further research in this field could include qualitative work with patient groups to further understand the effectiveness of patient information, both in terms of its quality but also its relevance. This could be expanded to include other sources of information such as video content and social media. Conditions should be considered individually as different approaches may be required for different groups of patients.
Researchers must take into account the dissemination of their work. Although patient involvement is increasingly prevalent in the research setting, conveying results in plain English could be further considered. Examples of this done well are the evide ntlyc ochra ne.net website, which aims to condense key Cochrane Reviews into plain English, 25 and the journal Frontiers for Young Minds, 26 which invites scientists to publish their work in a format suitable for schoolaged children. Open-access, plain English summaries of research findings would further empower patients in health care and should be considered by researchers and journals.
In conclusion, a systematic review of search engines found no evidence that was all of high quality, accurate and credible. It was also difficult to read. This is likely to disempower patients through lack of information, the opposite of their intentions in searching for information in the first place. Previous work has demonstrated that this is likely to be an issue across women's health. Healthcare professionals must take responsibility for producing better-quality information, as well as educating patients on how to determine the value of the websites they find.

AU T HOR C ON T R I BU T ION S
MH conceived the idea, planned the study, carried out and analysed the findings, and wrote the draft; FC planned the study and wrote the draft; CC planned the study and disseminated the patient questionnaire; AS planned the study and wrote the draft; LS planned the study, carried out and analysed the findings and wrote the draft. All authors approved the final manuscript.

AC K NO W L E D GE M E N T S
We are grateful to Anwen Gorry, MRCOG for her expert advice on the production and dissemination of high-quality patient information. We are also grateful to the women who have given time to help us understand priorities in patient information for PPROM, including women and their families affiliated with Little Heartbeats.

F U N DI NG I N FOR M AT ION
No funding was sought for this work.

C ON F L IC T OF I N T E R E S T S TAT E M E N T
MH, FC, AS and LS have no interests to disclose; CC runs the Little Heartbeats group for women with PPROM, and reviewed the 2019 RCOG Patient Information Leaflet When your waters break prematurely before its publication. Completed disclosure of interests form available to view online as supporting information.

DATA AVA I L A BI L I T Y S TAT E M E N T
The data that support the findings of this study are available on request from the corresponding author.

E T H IC S A PPROVA L
This study was carried out under the King's College London ethics number HR-21/22-28 751.