Public health importance of lead exposure

Lead is a non-essential element and exposure can cause adverse health impacts at any level [1, 2]. Lead exposure can result in symptoms such as abdominal pain, vomiting, loss of appetite, constipation, hearing loss, irritability and fatigue, developmental delay and learning difficulties [3]. Children are more vulnerable to the adverse effects of lead exposure as lead is likely to deposit and accumulate in their growing bones and organs [3].

Approximately 1 in 3 children–up to 800 million globally–have blood lead levels ≥0.24μmol/L (≥5μg/dL), at which concentration the World Health Organisation (WHO) [4] considers intervention is required. In the United States the intervention concentration has recently been lowered by the Centres for Disease Control and Prevention (US CDC) to ≥0.17μmol/L (≥3.5μg/dL) [5]. In England, the current blood lead concentration (BLC) which triggers public health intervention is ≥0.24μmol/L (≥5μg/dL) for both children and the developing foetus (pregnant women) and ≥0.48μmol/L (≥10μg/dL) for adults [6]. The intervention concentration for children was lowered from ≥0.48μmol/L (≥10μg/dL) to ≥0.24μmol/L (≥5μg/dL) from 5^th July 2021 [7] following a review published by Public Health England’s (PHE, now UK Health Security Agency (UKHSA)) Lead Intervention Concentration Working Group [1].

In the United Kingdom (UK), measures have been taken to reduce human exposure to lead though prohibiting the use of lead in petrol, paint, food cans and water pipes. However, historic circulation of lead-containing products and the importation of lead-containing products from outside of the UK still occurs [8].

There is no population level screening programme for lead poisoning in the UK. Screening for lead poisoning in asymptomatic children aged between 1 and 5 years is not currently recommended due to concerns relating to unknown prevalence of elevated blood lead concentrations (BLC) and complexity around testing and treatment of children [9]. Blood lead testing in the UK is therefore conducted on a case-by-case basis, often as part of generalised clinical investigations around pica behaviour (often associated with autism) or on clinical suspicion of lead poisoning. Due to the non-specific nature of symptoms, lead exposure can be missed or misdiagnosed. Blood tests for BLC in England are analysed by biochemical laboratories, predominantly at National Health Service (NHS) Supra-regional Assay Services (SAS) Trace Elements laboratories [10], or NHS Trust biochemical laboratory services [11].

The Lead Exposure in Children Surveillance System (LEICSS)

UKHSA’s Lead Exposure in Children Surveillance System (LEICSS) is a national, passive surveillance system for children residing in England aged <16 years who have an elevated BLC requiring public health action. There are currently 14 participating laboratories which send notifications of elevated BLC at a concentration reportable for public health action (currently ≥0.24μmol/L (≥5μg/dL)) to LEICSS (6 NHS SAS Trace Elements laboratories and 8 other NHS and private laboratories) [11]. All surveillance reporting laboratories are UK Accreditation Service (UKAS) accredited [11].

LEICSS team administrators will then send these notifications on to regional health protection teams (HPTs) for follow up and action based on UKHSA’s national standard operating procedure (SOP) for case management. HPTs may also receive case notifications for both children and adults directly from laboratories, health professionals treating the case or the UK National Poisons Information Service (NPIS) [12]. LEICSS extracts all notifications to HPTs of elevated blood lead in children aged <16 years in England for surveillance purposes, summarising case demographics in LEICSS annual reports [13, 14]. Further information on the surveillance processes and BLC testing regime is available in these reports.

Study rationale and aim

Whilst case demographics are described in LEICSS annual reports [13, 14], a detailed review of exposures, public health investigations and case outcomes for children with an elevated BLC reported to HPTs in England has not yet been conducted. Understanding these factors can give an insight to population level characteristics of exposures, risk factors and outcomes which helps to inform public health intervention, prioritise areas for prevention efforts and improve case management for child cases of elevated blood lead in England.

Data collection

For cases reported to HPTs between 1^st January 2014 and 4^th July 2021, a lookback questionnaire was sent to case managers to collect information on case demographics (age, sex, ethnicity), source of notification, household details, public health investigations (details of site visit, likely source and setting of lead exposure), pica, control measures implemented, outcomes and clinical care cases received. This required a manual review of the case records in the HPT case management system (HPZone). For cases reported to HPTs between 5^th July 2021 and 30^th September 2022 (end of data collection period), we used data collected within a live enhanced surveillance questionnaire (ESQ). The ESQ is currently used to support initial case management by collecting data on case demographics (age, sex, ethnicity), previous testing, history of pica or learning difficulties, occupational status/school attendance and hobbies, home ownership and likely sources of lead exposure.

Data from both questionnaires were extracted from Select Survey on 30^th September 2022.

Case definition for inclusion in this study

The case definition for inclusion in this study was:

Residents of England, aged <16 years at the time of the first elevated BLC, reported to UKHSA HPTs between 1st January 2014 and 30th September 2022 with a BLC reportable for public health action (≥0.48μmol/L before 5th July 2021 and ≥0.24μmol/L from 5th July 2021) where BLC is known, with a completed lookback questionnaire or with a completed ESQ. All data processing was conducted in R (version 4.2.2) and MS Excel.

Data deduplication and cleaning

For both datasets, a unique identifier was created using case first name, last name and date of birth. Duplicate records on unique ID were then manually reviewed in Microsoft Excel to ensure only unique cases were retained. Data were cleaned to meet the case definition as above.

Data management and recoding of variables

Data from the ESQ and lookback questionnaires were merged to form one summary dataset. Questions unique to the audit questionnaire and ESQ were summarised separately.

Any free text responses were manually reviewed and re-coded to pre-existing categories used in the questionnaires or added as a new category if not already accounted for. Responses to lead exposure through drinking water and/or lead pipes were combined to form a single variable ‘drinking water’, reflecting exposure through either source.

A deprivation variable was created for each case using an online tool [15] which matched postcodes to the Office for National Statistics (ONS) [16] 2019 indices of multiple deprivation (IMD) decile in Microsoft Excel. IMD ranks small geographical areas in England from most deprived to least deprived in 10 equal groups based on different domains such as income deprivation, education deprivation, employment deprivation and crime [17].

Data analysis

Categorical variables of interest were simplified and summarised as numbers and/or percentages of the total number of cases or subset of cases, where applicable. Continuous variables (age and BLC) were summarised by calculating median and inter quartile range. Any associations between cases and IMD decile were tested using appropriate regression techniques.

Ethics statement

No ethics approval was required for this study. All data were collected within statutory approvals granted to UKHSA for public health disease surveillance and control. Information was held securely and in accordance with the Data Protection Act 2018, General Data Protection Regulations (GDPR) and Caldicott guidelines.

Data cleaning and deduplication

Between 1^st January 2014 and 30^th September 2022, 521 children aged <16 years and resident in England were reported to HPTs for public health investigation for lead exposure. Post data deduplication and cleaning, 340 cases (65%), had either a completed lookback questionnaire or ESQ completed and met the inclusion criteria for this study. For cases eligible for a lookback questionnaire, 241 (80%) had one completed and for cases eligible for an ESQ, 99 (45%) had one completed.

Source of case notification and case demographics

Most cases were reported to HPTs by LEICSS (65%) followed by a paediatrician (16%, Table 1). HPTs also received case notifications from other sources such as direct reporting from non LEICSS laboratories, hospitals, and general practitioners (Table 1).

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Table 1. Source of notification and demographics of cases (n = 340).

https://doi.org/10.1371/journal.pone.0304866.t001

Fig 1 shows the distribution of cases by IMD decile. There was a general decrease in the percentage of cases with increasing IMD decile, with most cases (n = 106, 31%) categorised as IMD decile 1 (most deprived decile) and 59% of cases (n = 201) within the most 3 deprived deciles (IMD deciles 1 to 3, Fig 1). We found an exponential decreasing trend in cases by IMD decile (p <0.001).

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Fig 1. Percentage of cases by indices of multiple deprivation (IMD).

Percentages reported are of the combined dataset (n = 340). IMD 1 = Most deprived decile, IMD 10 = Least deprived decile. P-value for trend (<0.001).

https://doi.org/10.1371/journal.pone.0304866.g001

Case age ranged from 0 to 15 years with most cases aged 1–4 years (53%, Table 2). The median age for cases was 3 years. Cases were predominantly male (69%). BLC for cases ranged from 0.24μm/L to 17.59μm/L and the median BLC for cases was 0.65μm/L (lower quartile 0.50; upper quartile 1.03) (Table 1). Ethnicity information was largely missing (61%, Table 1) but where captured, predominantly White British (16%).

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Table 2. Likely setting and source of lead exposure, and risk factors for lead exposure in cases.

https://doi.org/10.1371/journal.pone.0304866.t002

Likely setting and sources of lead exposure

The most common setting where lead exposure occurred was within the domestic setting (92%) although other settings were identified (schools, hostel, parental workplace, and shooting (gun) club, Table 2). A specific exposure source was found in 61% of investigations, but only confirmed (likely by environmental sampling) in 16% of cases (Table 2). Despite this, the most common sources of lead exposure were paint (43%) and soil (29%), although other sources were identified which included drinking water/pipes, food (including, but not limited to spices, where further detail was provided), traditional (alternative) medicines, ceramics, cosmetics and lead weights (Table 2). Where traditional (alternative) medicine use was mentioned as a possible source of lead exposure and ethnicity information was also available (n = 10), 50% (n = 5) were of Asian ethnicity, although this should be interpreted with caution as case numbers were low. The majority of cases had pica (76%) and 60% had a learning difficulty (Table 2). Cases more often lived in rented homes (63%) with social rentals (48%) (council/local authority landlord and housing association landlords, being more common than private rentals (37%) (Table 3).

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Table 3. Public health and clinical investigations and outcomes for cases.

https://doi.org/10.1371/journal.pone.0304866.t003

Public health and clinical investigations

A site visit was conducted for almost half of cases (49%) of which the majority (87%) were conducted by public health or environmental health staff at the local authority, with PHE/UKHSA staff attending 36% of the time (Table 3). Other stakeholders that took part in site visits included water companies, housing teams, other local authority staff, clinicians, private surveyors, and interpreters (Table 3).

Control measures were undertaken for 71% of cases of which the most commonly recorded was advice (72%) followed by alteration to the home environment (37%, Table 3). Rehoming was mentioned in 8% of cases. Where known, cases tended to be under paediatric/paediatric outpatient care (63%, Table 3). A small proportion of cases were hospitalised (5%), received chelation therapy (3%) or were admitted to an accident and emergency department (1%).

Problems experienced during case investigations

There were 123 free-text responses out of total of 241 records (51%) entered for the question “Were there any specific problems or issues that arose during the investigation and management of this case?” in the lookback questionnaire. Of these, 8 (3%) explicitly stated no problem was experienced during investigations whilst 14 (6%) were free-text entries that were deemed unrelated to the question or did not fall into a theme.

The thematic analysis highlighted poor engagement by stakeholders or delays in response relating to case investigations, particularly relating to the parent/guardian (38%) and the local authority (15%) as the most frequently experienced problem during case management by HPTs (Table 4). This theme was different to that of contacting stakeholders (9%) which reflected difficulty in getting in touch with stakeholders specifically. Difficulty in agreeing or having clarity on roles and responsibilities was the next most frequently experienced problem experienced (13%). Specific examples given related to the following: refusal of testing possible lead exposure sources (including water) by local authority/environmental health, refusal of carrying out repeat blood tests by clinicians, responsibility for carrying out remedial work, agreeing on who should notify the case’s family of results, confusion around who needs to complete the questionnaire (presumably ESQ) with family (environmental health officer vs clinician) and who was responsible for continued enforcement of actions and case follow-up. Additional resource was required during case investigation. This involved the need for an interpreter, funding to conduct remedial work, and the need for additional expertise to support case management.

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Table 4. Problems experienced during case investigation.

https://doi.org/10.1371/journal.pone.0304866.t004

Case demographics

Demographics of cases included in this study were consistent with previously published findings [19–23] with cases predominantly being male, aged between 1–4 years old and having pica or a learning difficulty. The median BLC of cases included in our study (0.65μm/L) was higher than the BLC of laboratory detected cases in 2022 (0.37μm/L) as described in the most recent LEICSS annual report [24]. This was to be expected as the majority of the cases included in our study (71%) were those notified before the lowering of the public health intervention BLC in England on 5^th July 2021 [7].

Household tenure

Sixty-three percent of cases lived in homes that were rented, of which most, were social rentals (council/local authority and housing association, 48%). The proportion of rentals in our cohort was greater than the national average. The English Housing Survey 2021–2022 highlighted 36% of households were rented in England during this time period [25]. Both the proportion of social (48%) and private rentals (37%) in our cohort were greater than the national average (17% and 19% respectively) [25]. The rental sector overall, including social and private landlords, should be key targets for public health messaging and engagement regarding lead exposure and risks of lead exposure to enable case investigation and removal of sources, particularly as engagement, contact and worry of reaction of landlords/housing authorities were identified in the thematic analysis of problems occurring during case investigation. Additionally, the private rental sector in England tends to be poorly managed and with lower standards [26]. Although originally intended to provide short-term, flexible housing for mobile workers, it has become the dominant housing tenure for poorer young adults and their children. In 2017/18, one in three children in poverty lived in private renting [26]. However, as approximately one-third of our cohort lived in owner-occupied homes, it is important to consider the needs of this group too, particularly as the ability to undertake remedial action may be further limited due to lack of access to funding for this group.

Ethnicity and deprivation

Previous studies in the UK have shown children with an Asian ethnic background had higher BLC than children with European ethnicity [27], whilst data from the United States (US) has shown non-Hispanic Black children have higher blood lead levels than non-Hispanic White children [28]. Unfortunately, ethnicity data were largely missing in our cohort hence it is not possible to draw any valid conclusions on the ethnic makeup of the cases managed by HPTs in England.

Cases tended to live in the most deprived areas of England based on IMD decile. This could be a result of ascertainment bias as we may expect more cases to live in deprived areas. Deprived areas are more likely to have older, poorly maintained housing. Consequently, there is a greater exposure risk from leaded paint or lead pipes, with poorer conditions making these lead sources more accessible. Additionally, those living in more deprived areas, are likely to experience health deprivation and therefore, seek health and support services, and consequently be more likely to have elevated BLC detected through clinical investigations. The association between lead exposure and social deprivation has also been seen in other populations [29, 30]. However, some studies have not identified a relationship between IMD quintiles and BLC [31].

In England, there is a clear link between ethnicity and deprivation. In 2019, those with Asian ethnicity were more likely to live in the most deprived 10% of neighbourhoods in England (15.7%) followed by Black ethnicity (15.2%) based on IMD [32]. Having more complete and better quality ethnicity data for cases of elevated blood lead in England could support with identifying ethnic groups most vulnerable to lead exposure and help target public health messaging and action to reducing health inequalities for these groups.

It is also important to consider the association between socio-economic status, demographics, culture, religion, spirituality, and ethnicity with sources of lead exposure. For example, the use of ingestible complementary and alternative medicines (CAM), which may contain lead and other metals, may vary across different populations [33]. In our study, traditional (alternative) medicine was mentioned as a possible source in a small number of cases, however, the paucity of ethnicity data in our cases meant we were unable to explore associations between ethnicity and sources of lead.

Setting and sources of exposure

In this study, lead exposure occurred almost exclusively in the domestic setting (92%). However, other settings where lead exposure may have occurred were also identified such as schools, a hostel, the parental workplace, and a shooting (gun) club.

Although the use of leaded products such as paint and water pipes in the UK has been prohibited [8], old lead containing products may still be in circulation and the data from this study indicate that lead paint (43% of cases) or leaded pipes (less commonly) are still key exposure sources in the UK. In our study, case investigations found sources of lead for 61% of cases. For the rest, a sizable proportion did not have sources confirmed or suspected, and therefore, the significance of lesser-known sources of lead should not be dismissed when interpreting this data and during case investigations. For example, a recent study of lead concentrations in a range of environmental samples from households in Georgia found that along with paint, soil and dust, spice samples had some of the highest lead concentrations [34]. The role of the ESQ is designed to explore all possible sources and prompt investigators to ask questions on all potential sources and activities. In this study, where asked, 43% of cases knowingly lived in homes built before 1970, whilst 28% did not know and therefore, this percentage could be underestimated. Studies in England [31] and internationally [35–37] have identified housing age as a risk factor for lead exposure or higher BLC. Published literature tends to focus on household characteristics (age, type) as a proxy for exposure to household sources. However, these studies lack a more detailed breakdown of household characteristics or review of case investigations to describe the most likely activities or sources of lead exposure. It would be beneficial for further studies to conduct case reviews to add to the body of evidence for likely sources of lead exposure.

Identification of lead exposure sources using sampling is difficult and not always done. Source confirmation should occur through environmental sampling (i.e., taking samples of paint, soil, water, food, spices, etc, from the home) or use of more sophisticated identification techniques such as Lead Isotope Ratio analysis [34, 38]. Although the source of lead was only confirmed in 16% of cases in our study, there are a number of factors that impact on whether environmental samples are taken and tested. Sampling is expensive and there is often a lack of clarity around the responsibility for funding sampling. HPTs may also take a pragmatic view regarding source confirmation. If a potential source has been identified in the initial discussion with parents, advice on remediation is given and there is subsequently a consistent fall in BLC, the additional expense of sampling would be seen as unnecessary. Often environmental sampling is only carried out if there is some doubt about the source of lead. The outcome of the investigation needs to clearly result in a reduction in BLC to ensure that the exposure source has been removed. Repeated BLC testing and environmental sampling may be needed if this is not achieved.

Public health, clinical investigations, and outcomes

Almost half of all case investigations required a site visit and multiple stakeholders conducted site visits reflecting both the burden and multidisciplinary nature of case investigations. Advice was the most frequently mentioned control measure in this study, highlighting the importance of education and health messaging in managing cases and working with stakeholders to ensure the removal of exposure sources. Responsibility of enforcing agreed actions and continued follow-up was also highlighted as a problem in the thematic analysis.

Cases of elevated blood lead pose a burden on our National Health Service (NHS) and the provision of health care services and there is no minimum threshold for the adverse effects of lead exposure [1, 2]. Therefore, preventing initial and continued exposure to sources of lead are likely to help reduce referral of cases into secondary care. Exposure to lead can “damage the brain and nervous system, lead to slowed growth and development, learning and behaviour problems and hearing and speech problems” [39] which will mean a child is likely to need additional support throughout their life course for example from clinicians, speech and language therapists and educational support staff. In this study, most cases were under paediatric/paediatric outpatient care (63%). However, the primary reason for paediatrician referral is unknown, and it is important to also consider that the majority of cases in our study had pica or a learning difficulty, conditions which may also require paediatric care. Additionally, iron deficiency is associated with lead poisoning with both conditions sharing many of the same risk factors [40]. Although 8% of cases received ‘treatment’, due to the format of the question in its respective questionnaire, it is unclear what ‘treatment’ was received by cases, and this does not reflect a mutually exclusive category of care/treatment. Additionally, in our study, only 8% of cases had recorded repeat blood tests. Repeat blood testing should be undertaken for all cases referred to HPTs according to UKHSA’s national standard operating procedure (SOP) for case management, to ensure BLCs are below or reducing towards the intervention concentration. Due to the format of this question in its respective questionnaire, our findings are suggestive of poor data quality (as this information may not have been noted in the case’s record) or poor recall and should be interpreted with caution. Anecdotally, 88% of 48 cases managed in the North East and North Central London HPT in the last 5 years have at least one repeat blood test recorded–further suggesting the issue may be lack of recorded data rather than lack of testing. It is recommended that clinicians follow re-testing advice provided by UKHSA’s national SOP for case management–as in the absence of source identification, re-testing enables verification of source mitigation.

As well as the support needed by children for the management of symptoms and pathophysiology of lead exposure, the detrimental effects of lead exposure can impact a child’s educational outcomes and therefore have a subsequent effect on employment opportunities and in the longer term, socio-economic status. There is a strong body of evidence highlighting the relationship between lead exposure in childhood and violent crime in adulthood [41, 42].

Problems experienced during case investigation

The problems experienced during case investigation highlight the complexity in the management of cases of elevated blood lead. Stakeholder engagement/response was the biggest challenge experienced during case investigations (38%). It would be important to consider how engagement/response of HPTs, local authority colleagues, housing authorities/landlords, parents/guardians, and laboratories could be improved. Raising awareness of the public health importance of lead exposure, and the importance of timely action to reduce detrimental health effects in children could be one way of doing so and should be considered via outreach work, networking or national campaigns/awareness raising events. Alongside this, targeted public health messaging and engagement with housing bodies, both social and private, would be beneficial, particularly as parent/guardian worry over the reaction of the housing association to further investigation of the home by public health officials was identified as a problem in the thematic analysis. Other studies have also highlighted challenges in requesting testing and mitigating lead paint exposure by landlords [43].

Difficulty in agreeing or having clarity on roles and responsibilities was also a common theme emerging from the thematic analysis. Although this may be more difficult to do amongst all stakeholders that may be involved in case management, having guidance and signposting documents regarding roles and responsibilities will help.

Some cases may live in complex and vulnerable circumstances, reflected in the identification of safeguarding issues during case investigation. In the context of children, safeguarding reflects “the action that is taken to protect the welfare of children and protect them from harm” [44]. Involving stakeholders such as social services and support services adds complexity to what is already a lengthy and involved response.

Limitations