Breastfeeding assessment tools for at-risk and malnourished infants aged under 6 months old: a systematic review

Introduction

Protecting breastfeeding has been described as the single most effective child survival intervention (UNICEF, 2009; WHO, 2007). It also plays a key role in reducing the global burden of undernutrition (The Lancet Series, 2008) and is one of 13 priority interventions highlighted by the international ‘Scaling Up Nutrition’ movement (SUN, 2010). Despite this, suboptimal breastfeeding practices are common, accounting for significant morbidity and 804,000 deaths per year - 11.6% of all deaths in children aged under 5 years worldwide (Black et al., 2013). The greatest burden of mortality and morbidity is in low income countries as defined by the World Bank (Fantom & Serajuddin, 2016). High background mortality and high rates of undernutrition and communicable disease all make the protective effects of breastfeeding critical. With collapses in infrastructure and normal societal networks, emergency affected populations are particularly vulnerable if breastfeeding is not supported and problems are not quickly identified and addressed. A group particularly higher risk of mortality and morbidity are the small and nutritionally at risk infants under six months of age compared to the infant that achieve optimal growth. At a population level, small and nutritionally at risk children are those identified as wasted, stunted and underweight and a combination of these (ENN/LSHTM, 2021).

Whilst the importance of breastfeeding is widely recognised, supporting it can be challenging. Under the overall heading of ‘Promoting proper feeding for infants and young children’, the World Health Organization (WHO) lists several areas of work including: the Baby-Friendly Hospital Initiative (BFHI) (WHO/UNICEF, 2009a); promotion of exclusive breastfeeding; and the International Code of Marketing of Breast-milk substitutes. These initiatives are aimed at population level breastfeeding support; there is good evidence of their effectiveness (Beake et al., 2012). More challenging is how to help those who fall through these population ‘safety nets’; when an individual mother-infant pair presents with an established problem. Managing very small infants, those with growth failure and other high-risk characteristics is particularly complex. Breastfeeding problems are common in this group but there are many other potential underlying causes and contributory factors (Goh et al., 2016). Breastfeeding problems may be a primary cause or secondary to other causes. There is also a wide and complex spectrum of breastfeeding problems ranging from a simple positioning difficulty leading to insufficient milk intake, milk insufficiency perception, early complementary feeding introduction, to secondary milk insufficiency due to maternal depression, due in turn to lack of social support at home (Amir & Ingram, 2008; Moore et al., 2012; Pannu et al., 2011; WHO/UNICEF, 1994).

This review arose from a project exploring the Management of (Nutritionally) At-risk Mothers and Infants aged under 6 months (MAMI) Project (ENN/UCL/ACF, 2010b). The goal of the original MAMI Project was to investigate the management of malnourished infants under six months of age in resource-poor and humanitarian settings, and to contribute to evidence-based, better practice guidelines to improve practice. The project identified that the burden of infant less than 6 months’ undernutrition is significant: worldwide, 3.8 million infants are severely wasted; 4.7 million are moderately wasted (Kerac et al., 2011). Since breastfeeding difficulties are associated with undernutrition (Gagliardi et al., 2012; Gribble et al., 2011) (Gribble et al., 2011) and exclusive breastfeeding in infants under 6 months, a common treatment goal (ENN/UCL/ACF, 2010a), the report also examined breastfeeding assessment as part of overall infant assessment. It found no ‘gold-standard’ breastfeeding assessment tool that catered for inpatient and community settings. This is a critical gap; correct ‘diagnosis’ of a breastfeeding problem is vital to inform appropriate support and treatment. Building upon and updating the work of the MAMI Project, this current review thus aims to: a) identify and profile currently available breastfeeding assessment tools; b) discuss their potential application for assessing at risk and malnourished infants under 6 months (i.e. to determine the link between breastfeeding problems and malnutrition in a particular individual; to describe the nature of that breastfeeding problem). Informed assessment is critical to targeted intervention of support.

Methods

Breastfeeding assessment tools were defined as: documented guidance for clinicians, nurses, midwives, community health workers and carers on how to observe and/or assess the breastfeeding outcomes. These could take the form of checklists, questionnaires, algorithms, indices, history taking forms or listing of the specific aspects of breastfeeding that should be assessed.

Inclusion criteria: We included articles that: tested or used breastfeeding assessment tools; integrated at least one clinically relevant maternal or child outcome (e.g. duration of breastfeeding, infant weight gain); reported on tool performance. Articles describing complex interventions that included breastfeeding support could only be included if it was clear which tool had been used, and if breastfeeding assessment had been explicitly mentioned in the intervention description. There were no study design restrictions.

Exclusion criteria: Tools that focused just on artificial feeding (i.e. use of a breastmilk substitute) or that were designed for women after breast augmentation/reduction surgery were not considered in this review. Also excluded were tools that involved complex and expensive technology that are not designed for routine clinical use in resource poor settings (e.g. those using electromyographic methods; direct measurements of breastmilk composition; web-based tools; software to measure sucking strength/effectiveness; ultrasound measures of milk removal/swallowing). Tools that focused on wider breastfeeding support (e.g. employer support) rather than the actual process of breastfeeding were also excluded as were those focused solely on change in health worker knowledge, attitude or practice as an outcome. The literature search was restricted to English language articles with human subjects.

Databases and search terms: Articles were identified by searching electronic database Medline and Embase via Ovid interface (full search strategy is free available at http://www.doi.org/10.17037/DATA.00001881 in Extended data (Kerac et al., 2020)). Key words and MeSH terms were selected by the review on The Lancet Breastfeeding Series (The Lancet Series, 2016) and a recent similar review on feeding assessment tools (Howe et al., 2008). We also included hand search papers form grey literature, WHO and ENN websites. Searches were finalised in March 2018. This updated an earlier search done as part of the original MAMI project performed on PubMed, Web of Knowledge, Cochrane Review, Eldis and Google scholar databases which concluded in November 2013. In that original search, highly relevant journals were also searched directly: Maternal and Child Nutrition, International Breastfeeding Journal, Journal of Human Lactation, and BMC Family Practice. Reference lists and the ‘related articles’ were used to identify further articles. A standard two-stage search strategy was used: initial screening of titles and abstracts by 3 authors (C.B, K.L.R. and M.K.); detailed review of full articles secondly (C.B, K.L.R. and M.K.). Since tools were few but varied, risk of bias was not formally scored for each individual study but is discussed under ‘limitations’ for studies as a whole.

Results

From a total of 15,649 titles and abstracts screened, a final count of 52 papers describing 29 distinct breastfeeding assessment tools were identified (Figure 1).

Figure 1. PRIMA Flow diagram: Systematic search for BreastfFeeding Assessment Tools Review.

Preferred Reporting items for Systematic Reviews and Meta-Analyses (PRISMA) diagram of literature search results. Diagram retrieved from: http://prisma-statement.org/PRISMAStatement/FlowDiagram.aspx.

Discussion

Our review identified a number of breastfeeding assessment tools which could be used in the management of our target group of at-risk and malnourished infants aged under 6 months. Though none of the tools were developed for or tested on this group directly, characterising them and understanding the underlying evidence-base allows for better informed decisions about which might be the most helpful for future programme use.

Regarding the coverage of breastfeeding domains, only one tool (BEET) achieves full coverage of all the key assessment domains, but there were no validation study at our knowledge. The tools that achieve the widest coverage (IFE Module 2, BEET, and WHO/UNICEF B-R-E-A-S-T-Feed Observation Form and UNICEF/WHO Breastfeed Observation Aid) are generally those which have been developed with resource-poor low and middle income countries in mind. Although these tools are based on extensive clinical and field experience, they suffer from lack of validation research and miss some important domains (e.g. WHO/UNICEF B-R-E-A-S-T-Feed Observation Form misses health of the baby, IFE Module 2 misses positioning). These shortfalls could be addressed with minor modifications in the short term and with appropriately designed studies soon after to help determine which domains are the most important and relevant to patient care. Only 11 tools assess mothers’ own behaviour towards the baby: this is telling about her psychosocial status and can inform management. It is important to consider and account for such gaps since an infant may be effectively breastfed but at risk and malnourished for another reason, e.g. related to child health status or maternal factors. The mother-infant dyad is at the heart of approaches to treat malnutrition, but wider family and community relationship are also important but cannot be treated extensively in this review (ENN/LSHTM, 2021b).

A challenge validating breastfeeding assessment tools is the lack of a ‘gold standard’ treatment option for at-risk and malnourished infants less than 6 months. This makes validation studies a challenge methodologically since it is difficult to separate out the performance of an assessment tool from the effectiveness of the subsequent management strategy in averting adverse nutrition/morbidity outcomes. It is likely that different tools and different levels of management will be appropriate to different settings, e.g.

No single tool meets all these needs. Which tool is more appropriate to a given setting and individual mother-infant situation is itself an important question that warrants further testing and exploration.

For immediate use, whilst refining current tools and developing new future ones, the WHO/UNICEF B-R-E-A-S-T-Feed Observation Form, the aids in Module 2 on IFE and UNICEF/WHO Breastfeed Observation Aid, offer the most promise for programmes targeting at-risk and malnourished infants aged under 6 months.

In future research testing current and new tools, there is a need to agree on the most appropriate outcomes for validation studies targeting at-risk and malnourished infants under 6 months. The fact that so many tools exist, and that they cover such a wide range of feeding outcomes and domains arguably reflects uncertainly and lack of consensus about how best to assess the effectiveness of breastfeeding. For example, must there always be sufficient infant weight gain associated with other measures of effective feeding? Most current evidence comes from high-income countries and hospital settings. For use in tackling the significant global burden of malnutrition in infants aged less than 6 months, this is a problem. More tools for low income countries and for community settings are urgently needed (Moran et al., 2000; Mulder, 2006; Riordan, 1998; Riordan & Koehn, 1997).

Another key finding of our review was the variable - and overall low - quality of evidence underpinning existing breastfeeding assessment tools. Often the evidence-base for a particular tool is unclear, particularly their effectiveness in identifying specific breastfeeding problems and facilitating a resolution. Prospective and ideally randomised studies testing tools’ ability to do this are important in the future (Da Costa et al., 2008). Simple checklists have been shown to be powerful if used consistently in clinical settings (Haynes et al., 2009; Pronovost et al., 2006). There is therefore an argument to develop checklist-based tools that can be incorporated into routine breastfeeding assessment, to maximize the chances of resolving breastfeeding problems. These should also be able to discriminate between different types of breastfeeding problems and lead clearly to specific interventions.

We found that tools varied in their level of complexity, and their scoring systems. This may make individual tools relevant only for specific contexts. For example, three tools involve two stages: IFE Module 2 includes a simple rapid assessment, followed by a full assessment (ENN et al., 2007); the BFHI guidelines may include initial use of the breastfeeding assessment form, leading on to the UNICEF/WHO breastfeed observation aid if necessary (UNICEF, 2010; WHO/UNICEF, 2009a); the IMCI algorithm includes both a brief history taking and observations of the breastfeed (Mannan et al., 2008). This is potentially a good thing. Rather than one tool trying to do everything, different tools for different levels of assessment could be helpful: e.g. a quick, basic tool for use in the community to identify and correct ‘simple problems and identify referral need, complemented by a more detailed tool if problems are suspected or identified; another more detailed one for clinic/hospital use assessing more serious and complex problems flagged by the first tools. Tool developers need to consider what the key contact points with infants are, and the associated opportunities and capacities with these contact points. Coupled with this must be the capacity to respond to any problems identified. To address breastfeeding in high mortality/morbidity settings, tools need to consider not just physiological issues and techniques around breastfeeding, but also the wider social and psychological factors, which may be contributing to or perpetuating a problem (Galipeau et al., 2017).

Ways forward

As well as standard validation studies, new tools or those initially developed in/adapted from resource-rich settings should be assessed for cultural relevance and sensitivity before they are considered for use in resource-poor developing country/humanitarian settings. This formative work should ideally precede detailed validation or intervention studies. Validity is likely to vary according to target patient group and studies should therefore be sufficiently powered to explore subgroups. Tools that are designed to assess breastfeeding in healthy, well-nourished infants are not necessarily as good or adequate for assessing sick or undernourished ones. As none of those tools presented above were developed and tested in malnourished children and since these infants are at particularly high risk of morbidity and mortality, specific tools should consider the needs of infants aged less than 6 months with malnutrition – the group who inspired this review in the first place. Since there are many factors potentially underlying or contributing to malnutrition, we believe that tools for this group should be part of a wider assessment of the mother-infant dyad and take an appropriately broad perspective by considering other factors known to impact on infant nutrition e.g. maternal mental health, maternal illness, and maternal malnutrition.

Limitations

We acknowledge the limitation of our review. Firstly, it was restricted to articles written in English; there may be useful breastfeeding assessment tools published in other languages that were not captured.

Secondly, it is possible that we missed some studies, e.g. those using a broader approach to improving infant feeding may not have explicitly mentioned breastfeeding assessment tools as part of their intervention protocol; those which were using a tool in a programme but were not in the title or abstract clearly evaluating/testing the tool itself; those that may have had relevant content (e.g. maternal psychosocial status) but did not meet the inclusion criteria of one clinically relevant maternal or child outcome.

Third, we did not explicitly grade the quality of individual studies – this was felt not to add significant extra value to our review since observational studies, which comprised great majority of papers identified, are by definition low quality compared to intervention/RCT type designs. Quality grading would not have helped differentiate between more/less valuable tools, since the quality of evidence underpinning them all was generally low.

Finally, we found few tools explicitly targeted to our setting and main patient group of interest. This is not ideal since it means applicability had to be extrapolated based on our judgement rather than on hard data.

Despite these limitations, we do not believe that the overall direction or message arising from our findings are affected.

Conclusion

In this review of breastfeeding assessment tools for resource poor settings and targeting the assessment of malnourished infants less than 6 months, we have identified many possible but few stand-out ‘gold standard’ options. This represents an important evidence gap and highlights an urgent need for future research. The many different tools that we did find arguably show that one tool alone is unlikely to be suitable or even desirable. Tools must strike the right balance between simplicity, feasibility of use and minimal training requirements without losing the depth of information required to help healthcare workers and the women they are working with address breastfeeding difficulties. Thus, different tools for different levels of the health care system are needed: simple, quick-to-use tools for initial triage and problem identification in the community; more sophisticated tools for use in secondary and tertiary care settings where initial attempts at support have failed. Supplementary items such as pictures of good latch, and materials to help mothers and health workers understand the nature of breastfeeding problems (e.g. ‘take action cards’ (Dongre et al., 2010)), may be helpful. For any tool at any level, it is important that it leads to clear corrective actions. A “diagnosis” or “problem label” by itself is not always useful. Hence, future tools might give appropriate weight to problems, which can most readily be solved, or those which have the biggest short and long term impact. Research on breastfeeding assessment tools needs to consider such impacts – again, good test inter- and intra-observer validity is necessary but not alone sufficient to make a ‘good’ tool. It must help improve key outcomes like breastfeeding status and infant growth. Robustly designed studies in the contexts in which they will be used are essential.

Finally, we note that time will be needed to develop and test better future breastfeeding assessment tools. Yet support for women and their infants is urgently needed now. Not having an ideal tool is not a reason to defer breastfeeding assessment of at risk and malnourished infants under 6 months. There are great opportunities at present to collect and report good quality operational data using tools that are currently available. Expanding the current literature on breastfeeding assessment will be of great benefit to future tool developers. More importantly, focus on this area will also raise the profile of and directly benefit breastfeeding as a key child nutrition, health and survival intervention.

Data availability