Human Resources

Human resource issues were the most common barriers reported across the literature, mentioned by 41 of the 43 papers. Within this category, it would seem the greatest problems relate in one way or another to training of personnel, as this barrier was cited in 37 articles. There were several accounts of inadequate training resulting in fatalities or near-miss events. One woman, after being admitted with haemorrhagic shock, waited 36 hours before her abdominal pregnancy was diagnosed at laparotomy [24], Several studies reported that educational opportunities for health workers were overwhelmingly deficient due to the absence of continuing education programmes, adequate formal training and a habit of self-learning, as well as poor access to up-to-date educational resources [49], [53] [27], [61]. A Cameroonian midwife taking part in one of the studies remarked: “I am just happy with these few minutes we have spent today because for me this is my midwifery revision after 34 years”. She was the midwife in charge of a district hospital maternity unit [53].

The next most cited barriers were staff shortages, referenced in 26 articles, followed by staff motivation issues. Nineteen papers stated that low motivation caused delays. In one hospital in Côte d’Ivoire, the good will of administrative staff was a major factor in whether or not surgical kits could be purchased on credit for critically ill patients, despite the pleas of doctors [24]. Staff were variously identified as overworked and underpaid; [41] misusers of limited health resources for private practice [31]; lacking motivation to change the way they practise [49]. and down-right dishonest [42], [50]. Motivation levels often affected the availability of staff. Both doctors [29] and midwives [27] were found to be more motivated by their private practices, with low wages and poor conditions incentivising staff to work elsewhere, often in cities rather than rural communities [48]. One paper stated: “the staff had such a low salary that they could not concentrate on their work, but had to spend most of their time in income generating activities”. Such poor motivation was confirmed by medical officers as an important contributor towards poor patient management [54] and one article recommended that extra incentives should be put in place to retain staff in rural or marginalised areas [48].

Eleven of the articles suggested that 24-hour availability of staff was inadequate. Staff shortages and absenteeism almost certainly contributed towards cases of sub-optimal supervision (ten articles) and high workloads (six articles). Staff shortages were often compounded by managerial issues. In Gondar, Ethiopia, the region’s only obstetrician was often taken from the wards to teach and examine trainees [49], whilst in rural Gambia only one doctor remained on the unit because the other three had been allowed to go on leave at the same time [42].

Drugs and Equipment

Issues relating to the availability of essential drugs, equipment and blood were cited in 38 articles. Twenty-eight articles referred specifically to inadequate supply and distribution of drugs and equipment, compared with only eight that mentioned cost as a prohibitive factor. Twenty-two articles referred to essential equipment that was lacking altogether (including surgical equipment and vacuum aspirator pumps), as well as very basic equipment such as surgical gloves and cannulae. A further six articles made reference to existing equipment that was either broken or poorly maintained.

Lack of safe blood supplies for transfusion was also a major problem identified in 13 articles. In one Nigerian tertiary hospital over 20% of the maternal deaths were due to delays in acquiring blood [47]. In some cases, blood had to be obtained from hospitals that were several kilometres away [24]; had to be bought by the family at great expense [42], [50], or donated by relatives or friends [43]. Family members were often expected to embark on journeys to obtain blood products [27], sometimes taking several days [42].

Five articles stated that appropriate storage facilities for drugs and blood were not available, and so products became spoiled due to storage at incorrect temperatures. A national survey in Tanzania found that uterotonic drugs (which should be kept refrigerated) were stored at room temperature in 28% of the facilities [46]. During an interview, one Gambian woman recounted, “My husband managed to buy two bottles of blood for me yesterday. The morning ward staff collected the blood from the lab and put them on top of the ward refrigerator for cooling. The following morning my husband was again told to replace the two bottles as the previously acquired blood was ‘spoiled’ as the nurse put it” [43].

Finally, in three articles, key drugs were either missing from the country’s ‘essential medicines list’, or not registered for a particular indication. This was a particular issue for magnesium sulphate. For example, in one study, the drug was not licensed for the treatment of pre-eclampsia in 7 out of 13 low-income countries [34]; in Zimbabwe, it had not been registered for use at all [52]. One reason offered was that the low cost of the drug removes any incentive on the part of manufacturers to maximize its use [52].

Guidelines/policy

Twenty-nine of the papers identified inadequate clinical guidelines or poor policy environment as a factor contributing to sub-standard maternal care in the population being studied. Issues relating to poor policy at the level of the individual facility (for example, bad record keeping) were reported in 14 articles. One of the most common examples of poor policy at the hospital level was the lack of partogram use, which was specifically mentioned in five articles [49], [58], [61], [64], [65]. In one hospital, staff understood the importance of using partograms to monitor the progression of labour but were left to make their own bespoke charts in the medical notes as the hospital did not supply them [49]. Another example was cited in Nairobi, where a policy which dictated that all patients must obtain antenatal cards and pay cash deposits before being eligible for delivery services led to recurrent treatment delays [58].

The inadequate content and dissemination/enforcement of national clinical guidelines was mentioned in eight and nine articles, respectively. The article by Aaserud et al. found that national clinical guidelines for pre-eclampsia were absent in eight out of 13 low and lower-middle income countries, leading to a failure to provide magnesium sulphate when necessary. Those based in Latin America expressed a contrary concern: the over-use of magnesium sulphate in situations in which it was not supported by the latest research, similarly indicating a failure to disseminate best-practice guidelines effectively [34].

Ten articles also reported that staff preferred to use less effective or non-evidence based interventions. These included a preference for expectant rather than active management of the third stage of labour [46]; treatment of eclampsia with diazepam [51] [53]; routine use of enemas [44], and a lack of compliance with recommendations to deliver HIV positive women routinely by Caesarean section [49]. In the article from Cameroon, one medical officer was quoted as saying “I not only don’t do it [external cephalic version (a recommended practice for breech presentation at term)]; I actively discourage it because it is very dangerous” [53].

Facility Infrastructure

Poor hospital infrastructure was identified in 25 articles and the most frequent barrier explicitly reported within this category was a shortage of power and/or water. Nine papers stated that such shortages delay treatment in emergency situations.

Orji et al. concluded that the major factor causing delay to treatment is theatre-related [47]. Indeed we found six studies, which explicitly stated that theatre space and surgical facilities were a problem and a further ten that implied this. Not all hospitals have a theatre but even in those that do, surgical services may be irregular and not accessible 24 hours per day. Delays understandably occur when theatres are already being used, but even when extra theatre space is made available it is not always possible to mobilise staff and so treatment is delayed [24].

Another delay related to transfusion facilities. Many articles stated that the lack of blood delayed treatment, but eight papers found that a number of hospitals did not even have a blood bank. In one paper, only 9% of the district hospitals in Dar Es Salaam had a blood bank [54] and the proportion in another article looking at obstetric care in poor regions of Ghana, India and Kenya found equally poor availability [58]. Bed/ward space and laboratory facilities were less commonly problematic, with only four and two citings respectively.

Referral-related Factors

It is alarming that even when conditions are identified that require more sophisticated care, providers are sometimes unable to, or worse, unwilling to arrange referrals. Indeed one patient was not referred because of her HIV positive status [41]. Twelve of the 16 articles that highlighted referral-related issues reported that inadequate emergency transport contributed towards maternal mortality. Various reasons were cited such as the ambulance - had broken down and there was no replacement [42]; was being used for an alternative purpose [33], or was under-staffed and ill-equipped [27]. Car ambulances were only available in 7–31% of facilities in three districts of Malawi [28]. Further delays occurred in three of the papers because the ambulance had no fuel [33], [41], [42], meaning at times that the woman’s relatives had to be sent to purchase more [42].

Eight articles mentioned difficult journeys mothers undergo when referred to higher levels of care. Distances between facilities can often be great and the roads themselves poor. One article described the regional hospital as “about 2 hours away on paved roads” [41]. It was also noted that communication between facilities can be sub-standard. Five articles stated that communication was an issue because of non-functioning radios and telephones or a complete lack thereof.

Patient-side Factors

Thirteen articles reported that patient-side barriers contributed to maternal deaths once women reach a medical facility. Eight articles cited cost-related factors related to compulsory user-fees that hospital staff demand prior to providing treatment/surgery, particularly in relation to emergency Caesarean section. Religious beliefs and negative socio-cultural attitudes towards biomedicine were believed to impede the use of certain medical interventions in six articles. These interventions included HIV testing and administration of peripartum antiretroviral treatment, companionship during labour because of concerns about witchcraft, privacy and gossip [53], and taboos surrounding blood donation that prevented family members from providing or obtaining blood supplies for emergency transfusion [29], [59].

Strengths and Limitations

There were several limitations to this systematic review. First, a number of rich sources of information about the third delay may have been missed, for example unpublished facility-based audits and confidential enquiries into maternal deaths. Although we sought expert opinion to identify key publications in the grey literature, our search strategy largely identified articles published in peer-reviewed journals. Since many journals have an explicit policy of not publishing audits, a considerable amount of information about Phase III delays may have been missed.

Another problem encountered was related to defining appropriate search terms that would identify all articles relating to Phase III delays. For example, very few medical subject headings (MeSH) were available for treatment delays at the facility level. Instead, free-text search terms had to be developed. Articles about facility-level barriers to the provision of maternal health care do not necessarily refer explicitly to the ‘third delay’ or use other easily predictable terminology. Moreover, there are so many wide-ranging barriers that could impact upon the quality of obstetric care, that it was not possible to anticipate all possibilities in our search strategy. The sheer breadth of the topic means that some important original articles may have been missed. Despite these problems, we believe that although the overview of factors provided in this review is unlikely to be completely exhaustive of the literature on each barrier it is nonetheless a comprehensive review of the categories of barrier that contribute to Phase III delays.

A key challenge related to data extraction was that was that barriers were often poorly defined: for example, many of the articles attributed maternal deaths to the ‘lack of’ a specific drug or resource. With a few exceptions [24], [34], [52], the reasons underlying the poor availability or health commodities were not explored in any depth, making it difficult to classify whether the poor availability was due to cost, supply and distribution, or a combination of factors. Another common problem encountered was the ambiguity of the phrase ‘a shortage of adequately trained staff.’ Is the emphasis here on the number of personnel or the quality of their training, or both? For consistency, in such instances, we decided to record training as an explicit barrier and staff shortage as an implicit barrier.

In some articles, the root cause of poor quality of care was left entirely unexplained. For example, one article cited the case of a woman with diagnosed hand presentation who needed an emergency Caesarean section, yet was left for over 48 hours before having surgery. The authors gave no reasons as to why was she not attended to sooner by staff despite a correct diagnosis [42]. Was it a case of staff lacking the training to know that they should intervene? Was the doctor unavailable? Could the woman simply not afford to pay for the operation? Or were there other factors at work? We chose to document barriers separately that were implied in the text, but not clarified or discussed explicitly (Table 1, column 3).

The quality of the research in many of the articles was methodologically weak. Several papers also failed to explain their methodology adequately, yet made relevant observations that were worthy of comment. Whilst there are clear tools for the assessment of randomized controlled trials and other experimental studies, there is little guidance concerning analysis of the quality of qualitative observational studies. Although several assessment scales and checklists have been used [73], [74], they have not been validated and are inappropriate for non-intervention studies; thus, we included all studies that met the inclusion criteria, regardless of the quality of the quality of the methodology.

The results of this systematic review may be influenced by study bias: that is, the authors of the articles included in the review may have chosen (intentionally or otherwise) to investigate or report certain types of barrier over others, depending on their particular area of interest. Although current knowledge is very limited with regard to the influence of bias on systematic reviews without meta-analyses [75], we acknowledge that the frequency of barriers presented here are not necessarily representative of the “true frequency” of barriers in the developing world. The synthesis of results from the reviewed articles (i.e. the frequency counts in Table 1) should be interpreted with some caution, and not extrapolated to represent the true magnitude or relative importance of the various barriers in the developing countries.

The results of the articles are in fact very hard to compare due to the differences in study design, sampling strategy and the analysis techniques employed. Furthermore, context specificity means that synthesis is extremely problematic. As Gabrysch and Campbell highlight in their review of Phase I and II delays [9]:

“Even if all methods were identical, it would be naïve to expect the effect of, say, distance in Malawi and Peru to be the same, given that infrastructure, transport options, education level, norms around place of delivery and many other factors differ.”

As this review highlights, a highly complicated web of reasons, many of which are interdependent, can be used explain treatment delays, ranging from behavioural factors such as staff motivation to material factors such as the availability of specific resources. Many of these factors are hard to measure, often go unreported, and are therefore extremely hard to control for to allow context to be taken into account when synthesising results.

Finally, information about which barriers are more or less important to the provision of high quality care was rarely given in the articles reviewed. With the exception of one article [45], studies did not attempt to assess the magnitude of barriers in the local context. This type of assessment would be useful for both short- and long-term priority setting purposes. Efforts to incorporate cost-effectiveness into assessments would also be valuable.

Implications and Recommendations

From an economic perspective alone, global maternal health outcomes would be greatly improved if ways to overcome obstacles to the widespread use of currently available interventions could be found. This review highlights the importance of addressing both supply-and demand-side barriers in any effort to reduce maternal mortality. The studies included document the severity of facility-level failures and serve to highlight that a focus on patient-side delays can sometimes conceal the fact that many health facilities in the developing world are still chronically under-resourced and cannot cope effectively with serious obstetric complications.

Moreover, as Thaddeus and Maine state in their original article, the “three phases of delay rarely operate in isolation…indeed the factors are likely to be interactive and multiplicative. Thus, barriers and poor care encountered at Phase II and III feed back into subsequent decision-making at Phase I” [8]. For this reason, Phase III barriers are likely to influence decisions to seek care and impact not only on maternal mortality at the facility-level, but also on maternal deaths in the community.

The focus in the past few decades on encouraging a shift from home-based to institutional delivery will have been misplaced if efforts to improve the quality of care a woman receives once she comes through the doors of a health facility is not stepped-up. Indicators such as the ‘time from arrival to definitive treatment’ [76] or the ‘percentage of women with obstetric complications treated within two hours at a health facility’ [77] have been proposed. However, few studies reported these outcomes as the data are rarely available from routine medical records [24]. We agree with those who call for the introduction of benchmark indicators that assess the content and quality of maternal care, rather than the rates of skilled attendance at birth alone [78].

Simple, replicable tools to assess facility-level barriers are badly needed to assist health managers in identifying facilities that deliver sub-optimal care, and in both making and monitoring the required improvements. No generally accepted methodology exists and this makes comparisons between countries very difficult [19]. We commend efforts by Pitchforth et al. [49] to incorporate social science methodology into these evaluations, as using mixed-method designs may yield more useful results.

To ensure that information on barriers to high quality, effective care contributes to improved responsiveness to emergencies, specific reasons for delays in providing particular interventions must be identified. We have recently completed a large-scale survey of direct maternal healthcare providers in 99 developing countries in an attempt to link specific Phase III barriers to a range of recommended interventions, and to identify locally-appropriate solutions [79].

Conclusions

This review highlights how a focus on patient-side delays in the decision to seek care sometimes conceals the fact that many health facilities in the developing world are still chronically under-resourced and unable to cope effectively with serious obstetric complications. A wide range of facility-level barriers to EmOC are in operation which result in thousands of avertable deaths worldwide. At present, facility-level barriers are often not reported in sufficient detail in research studies evaluating the quality of maternal healthcare. This makes finding solutions very difficult. We stress the importance of addressing supply-side health systems barriers alongside demand-side factors if further reductions in maternal mortality are to be achieved. The development of simple, replicable tools to assess facility-level barriers should be seen as a priority for future research. The availability of such tools would assist health managers in identifying facilities that deliver sub-optimal care, and in both making and monitoring the required improvements.