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Optimal nutrition is important at all stages of life but assumes even greater importance in pregnancy. During pregnancy, nutritional requirements are increased and are critical in supporting the physiological adaptations that occur during pregnancy. In the absence of adequate nutrition, both fetal and maternal health can be adversely affected.

Due to the modulation of the immune system during pregnancy, pregnant women are more susceptible to foodborne illness. Thus, while the intake of adequate nutrients during pregnancy is imperative, so too is ensuring the avoidance of high-risk foods. The New Zealand Food Safety in Pregnancy guidelines, published by the Ministry for Primary Industries,1 provide a number of recommendations for safe eating in pregnancy. These include avoidance of foods that are high risk for the transmission of foodborne infections, including listeriosis and toxoplasmosis, and safe preparation and handling of foods. Listeriosis, caused by the bacteria Listeria monocytogenes, is of particular concern. L. monocytogenes has a predilection to affect pregnant women and neonates. Pregnant women, in particular, are at an approximately 18 times greater risk for infection than the general population.2 In resource-rich countries, L. monocytogenes has the highest case-fatality rate of any foodborne pathogen.3

Listeriosis in pregnancy encompasses maternal, fetal and neonatal disease. Listeriosis most commonly presents in the third trimester of pregnancy (from 28 weeks)4 and is rarely fatal in the mother, particularly in the absence of coexisting medical conditions.5,6 However, if transmitted to the fetus, infection can lead to miscarriage, pre-term delivery or stillbirth. In a recent study of 107 cases of pregnancy-related listeriosis in France, the rate of transmission of infection from the mother to the fetus was 96%, and major fetal or neonatal complications were observed in 83% of infected mothers.3

In New Zealand, lead maternity carers (LMCs), including midwives, general practitioners and obstetricians, are encouraged to provide written and verbal advice regarding food safety in pregnancy, and to reiterate this to women throughout pregnancy. A recent study in Australia reported that the majority of pregnant women have poor knowledge of food safety in pregnancy guidelines and continue to consume foods that put them at increased risk.7 Previous international studies have consistently shown suboptimal adherence among pregnant women to safe eating in pregnancy recommendations.8,9

Pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines, which differ from international guidelines to include foods appropriate for the typical New Zealand diet, has not been studied systematically. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines. Understanding knowledge and behaviour is important to inform the provision of antenatal care and to identify women who are at increased risk and may therefore benefit from more intensive advice and support during pregnancy.

Methods

This cross-sectional study of pregnant women in New Zealand, aimed to examine pregnant women’s knowledge of listeriosis and the New Zealand Food Safety in Pregnancy guidelines and associated eating behaviours.

Questionnaire development

A questionnaire was developed comprising of four broad sections: demographic data, knowledge of the Food Safety in Pregnancy guidelines, behaviours related to safe eating in pregnancy, and safe food handling practices. The questionnaire consisted of 69 questions and took approximately 15 minutes to complete. The Automated Readability Index (ARI) for the questionnaire was calculated according to the formula: 4.71 (characters/words) + 0.5 (words/sentences) – 21.43. The ARI was 5.2 (readability was deemed appropriate for an eight to nine-year-old).10

In questions related to food safety, participants were asked if they thought it was safe to eat each of 23 different foods in pregnancy. Foods considered included those from the New Zealand Food Safety in Pregnancy guidelines: identical wording to the guidelines was used, safe and unsafe foods were included, and foods were listed in a random order. The options ‘yes’, ‘no’ and ‘I don’t know’ were offered. Answers left blank were considered as missing data. To assess behaviours regarding safe eating, participants were asked if they had eaten a range of foods during their current pregnancy. Foods assessed were the same as those in the Food Safety in Pregnancy guidelines and answers were considered correct if they accorded with the guidelines. The options provided included ‘sometimes/often’, ‘never’ and ‘I don’t know’. Finally, we asked about food handling practices in pregnancy and whether participants’ behaviour was consistent with the recommended behaviours. Options provided included ‘always’, ‘sometimes’, ‘never’ and ‘not applicable’.

Pre-testing

Pre-testing of the questionnaire was completed at Christchurch Women’s Hospital (a tertiary care maternity hospital). Twenty women attending an outpatient appointment with an obstetric physician completed the questionnaire. Following pre-testing, no changes were made to the questionnaire, aside from minor changes to layout. Three obstetric specialists and two midwives were also consulted following pre-testing and no further changes were made.

Recruitment

There were two arms to recruitment. Participants were either recruited when attending antenatal clinics at Christchurch Women’s Hospital (hospital cohort) or via Facebook (online cohort). This study was advertised on Facebook pages that were targeted at pregnant women in New Zealand. The questionnaire was delivered via RedCap, a secure web application for managing online questionnaires. Women completed the questionnaire independently, either on iPads provided by the questionnaire coordinators, or on their cell phone or home computer. A recruitment rate was calculated for the hospital cohort as all women offered the questionnaire were counted. A recruitment rate could not be accurately calculated for the Facebook cohort.

Women were eligible to participate if they were currently pregnant, ≥18 years of age, and had sufficient English language literacy to complete the questionnaire. We asked that women had at least one antenatal appointment (eg, with a general practitioner, midwife or obstetric specialist) prior to participation in the study to allow an opportunity for food safety in pregnancy education (it is recommended food safety advice be provided at the earliest opportunity in pregnancy and therefore it would be expected that after a first appointment there should have been at least some advice provided). Recruitment was completed over 30 days in December 2017 and January 2018.

Statistical analysis

For each food included in this study, the proportion of participants who believed the food was a) safe to eat in pregnancy, or b) should be avoided, was determined. This provided an indication of participant knowledge. To determine adherence to the guidelines, the number of women who a) consumed the food (‘sometimes or often’), or b) never consumed the food, was also determined. This provided an indication of participant adherence to the guidelines.

A discrepancy score was calculated by determining the number of participants who correctly indicated that the food should be avoided in pregnancy yet reported consuming the food ‘sometimes or often’. A discrepancy score was only calculated for the foods that are unsafe to eat during pregnancy.

An overall knowledge score was calculated for each participant based on their knowledge of whether the listed foods were safe to consume. Participants were given a score of one if they responded correctly that a food should be avoided or was safe to eat, or zero if they responded incorrectly or that they did not know if a food was safe. An overall score was calculated by summing all 23 foods listed: a higher score indicates greater knowledge. An overall adherence score was also calculated using the same method, but only including the foods that are unsafe to eat during pregnancy (maximum score 13). Knowledge and adherence scores were converted to percentages by dividing overall scores by the number of questions answered. Participant’s missing more than two knowledge or adherence questions were excluded from the analysis. Multivariable linear regression models were used to investigate the characteristics associated with higher levels of knowledge and adherence. Participant ethnicity was based on self-report and prioritised according to New Zealand Ministry of Health guidelines.11

Māori consultation and ethics approval

Māori consultation was sought at the commencement of this project with a University of Otago Kaitohutohu Rangahau/Māori research advisor. This study was approved by the University of Otago Human Ethics Committee (Health), ethics reference number H17/143.

Results

Demographic characteristics of participants

In total, 205 women participated in this study; 100 from the hospital cohort and 105 from the online cohort. The recruitment rate for the hospital cohort was 98.0% (105/107). The characteristics of participants are presented in Table 1.

Table 1: Participant characteristics.

a Predominantly NZ European but also includes European, Middle Eastern, Latin American, and African.
b Locality breakdown not available.
c Includes Samoan, Cook Island Māori, Tongan and Niuean.
d Includes Indian.

The majority of participants were of European/Other ethnicity (74.5%), university educated (71.1%) and in their third trimester of pregnancy (53.2%). Nearly half (47.5%) of participants were primiparous. The median age of participants was 30 years (range 18.7–54.1 years).

Education about the Food Safety in Pregnancy guidelines

Participants reported most commonly receiving food safety advice from their midwife (n=144, 70.2%), family members (n=82, 40.0%), friends (n=81, 39.5%) or their general practitioner (n=67, 32.7%). The majority of participants (n=128, 62.4%) reported completing independent research (eg, on the internet or in books). Nearly three-quarters of participants 146 (71.2%) reported obtaining a copy of the New Zealand Food Safety in Pregnancy guidelines during their current pregnancy, of whom 126 (86.3%) reported reading them.

Concern regarding food safety and reasons to follow the Food Safety in Pregnancy guidelines

Over half of participants (60.0%) reported being ‘very concerned’ (12.7%) or ‘concerned’ (47.3%) about food safety in pregnancy, while 19.5% stated they were ‘neither concerned or not concerned’ and 20.0% stated they were ‘not concerned’. Participants who stated they were ‘very concerned’ or ‘concerned’ were most likely to be in their first (48.7%) or second (32.5%) pregnancy.

The majority of participants agreed that eating according to the Food Safety in Pregnancy guidelines supports maternal health (70.7%) and the health of baby (98.0%). Thirty-three participants (16.1%) also indicated that eating safe foods in pregnancy supports family health.

Knowledge and consumption of unsafe foods during pregnancy

Participant knowledge of the food safety guidelines is presented in Table 2. The most commonly incorrectly identified unsafe foods were cakes, slices and muffins that have added cream or custard (25.5%), hummus (20.6%), salads, including fruit salads, that have been made at a shop or café (18.2%) and cheese that is soft or semi-soft (15.1%).

Table 2: Participant knowledge of the Food Safety in Pregnancy guidelines and their behaviours related to the guidelines.

The most commonly reported unsafe foods consumed in participants’ current pregnancies included cheese that is soft or semi-soft (51.5%), salads, including fruit salads, that have been made at a shop or café (48.3%), dressings served at a restaurant or café, eg, mayonnaise, hollandaise (39.5%), cakes, slices and muffins that have added cream or custard (36.1%), and cold ham or other pre-cooked meat, like chicken and salami (34.2%).

A total knowledge score was calculated for each participant (Table 3). The median knowledge score was 95% (interquartile range [IQR] 83–100%). Only 25% (n=51) of participants answered all questions correctly. Higher average standardised knowledge scores were associated with having a higher level of education (p=0.003) and being of European/Other ethnicity (p=0.0062).

Table 3: Demographic and pregnancy-related factors associated with pregnant women’s knowledge of unsafe foods during pregnancy (knowledge score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised knowledge scores.

The median adherence score was 77% (Table 4; IQR=62–92%, range 7.7–100%). Only 12.9% of participants reported full adherence to the Food Safety in Pregnancy guidelines. Higher average adherence scores were associated lower parity (p=0.002) and having reviewed the Food Safety in Pregnancy guidelines (p=0.007).

Table 4: Demographic and pregnancy-related factors associated with pregnant women’s behaviours related to the Food Safety in Pregnancy guidelines (adherence score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised adherence scores.

Adherence to advice regarding safe food handling in pregnancy is detailed in Table 5. Only 20.1% of participants reported routinely cooking meats until steaming hot and 29.8% of participants reported that they never cook meats until steaming hot. Highest adherence was seen for washing surfaces, utensils and hands after handling raw meat and eggs (89.7%).

Table 5: Participants’ adherence to recommended safe food handling practices in pregnancy.

Discussion

This study identifies considerable gaps in pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines and incomplete adherence to this advice. The New Zealand Food Safety in Pregnancy guidelines are readily available to pregnant women in New Zealand, both online and in print, and have been for at least the past 12 years.

While it is encouraging to note that the average knowledge score across all participants was 95%, only 25% of participants answered all questions correctly, meaning three-quarters of participants incorrectly identified at least one unsafe food as safe to eat in pregnancy. Participants were more certain about ready-to-eat seafood and meats, raw eggs and unpasteurised milk, but were less certain about hummus and cream/custard. Variability in knowledge by food type is an expected finding12 and might reflect knowledge of food safety in general, as well as in pregnancy. For example, raw or undercooked meat and seafoods are known sources of several foodborne illnesses that have been the focus of public health campaigns in New Zealand.13

Knowledge is important, but it is behaviour that ultimately determines risk. Only 13% of participants reported complete adherence to the food safety in pregnancy guidelines. That there is often a poor correlation between knowledge and behaviour with regard to food safety has been reported several times previously.14–16 It is interesting to note the varied levels of compliance around raw seafood versus cold, pre-cooked meat and also the high level of consumption of store bought salads and soft and semi soft cheeses. Adherence to safe food handling behaviours was low overall. Only 20% of participants reported routinely cooking meats until steaming hot. Food handling and preparation are largely unconscious and routine behaviours and achieving behaviour change is known to be problematic in this context.17

In New Zealand, the overall risk of acquiring listeriosis is low. A recent study reported that in the 20-year period from 1997 to 2016 there were 147 cases of listeriosis in women and children that resulted in notification or hospitalisation.18 This study also reported that there had been little change in incidence over time. Despite this, during the period 1 January 2009 to 31 December 2018, L. monocytogenes was associated with the highest number of food recalls due to microbial contamination in Australia (who have a similar food environment to New Zealand). The commonest recalls were for meat (125 recalls), dairy (18 recalls) and processed foods (10 recalls).19 These are food groups for which participants reported poor adherence to the guidelines, both in terms of food intake and food safety-related behaviours. The available New Zealand data (http://www.mpi.govt.nz/food-safety/food-recalls/recalled-food-products) show a similar pattern, although contamination with L. monocytogenes is a less common reason for recall; just four out of 41 recalls in 2019 to mid-September, and none at all in 2018.

There are several reasons why food safety knowledge and adherence might not be optimal. Only 70% of participants reported receiving information from their midwife; 40% received advice from family or friends, and 33% received education from their GP. Further, 62% reported doing their own research. Healthcare providers have previously been identified as the preferred source of food safety advice.20,21 However, there might be inconsistencies in the messages being communicated, or difficulties in comprehension of information. Further contributors might include a lack of recall secondary to information overload in the antenatal period, underestimating risk due to a lack of experience with previous food-related illness, the convenience of high-risk foods overriding food safety advice, and balancing the need for a healthy diet versus the risk for listeriosis. From the perspective of providers of antenatal care, issues such as time constraints, insufficient22 or dated knowledge, or reliance on anecdotal evidence might be contributors.

While it is reported that those of a lower education level are more likely to engage with more risk-taking health behaviours, the same is also true for those of a higher education level. The empirical relationship between education and risk aversion appears ‘U-shaped’, where those with moderate amounts of schooling are the most risk averse.23 It is possible, therefore, that those in our study, who were overall well-educated, were making decisions regarding their own risk assessments, even if aware of the guidance. Other pregnancy-specific changes that might impact eating in pregnancy include food aversion, nausea and emotional eating.

Māori participants had lower reported knowledge of the food safety guidelines and also lower adherence to the guidelines. There are numerous reasons that this might be the case. Firstly, food safety guidance might not adequately reflect eating patterns or behaviours of Māori, for example a higher emphasis on communal food consumption.24 Lower levels of knowledge among those from higher risk groups has been reported previously.2 Health education resources need not only to consider the information they contain but also the way in which it is presented. For example, the current Food Safety in Pregnancy booklet1 features imagery of apparently Pākeha women and a pregnant woman eating alone. It is imperative detailed cultural consultation is included in future revisions of the guidelines.

Strengths and limitations

This study included women across a wide range of the community, including women with higher-risk pregnancies (members of the hospital cohort) and those participating in differing models of obstetric care (those under community midwives only versus those with the addition of specialist obstetric care, including obstetrician oversight, dietetic care and specialist midwifery care). The hospital cohort had a high recruitment rate of 98%.

All data were self-reported, and hence are liable to be affected by social desirability bias. For example, women may have reported not consuming particular foods if they knew that these foods should be avoided in pregnancy. However, participants’ responses were anonymous and were not collected by their obstetric healthcare providers so this might have reduced the impact of this source of bias.

Our sample had a higher proportion of participants with a university education than the general population (71.1% compared to 29.8% for the general population).25 In view of the lower average knowledge scores in participants with lower levels of education, the over-representation of women with a university-level education might mean that our study provides an overestimate of knowledge related to the New Zealand Food Safety in Pregnancy guidelines, and actual knowledge levels might be lower than we have found. We only included participants who self-identified as having adequate English language literacy to complete the questionnaire; this might limit the findings in those of ethnic minorities. Our sample had lower numbers of Māori and Pacific participants when compared to the general population of New Zealand.

Implications

The findings of this study indicate that the majority of participants did not have complete knowledge of the New Zealand Food Safety in Pregnancy guidelines. Provision of information regarding high-risk foods and high-risk behaviours related to the safe handling of food should ideally take place at the first antenatal appointment when the threat to fetal health due to L. monocytogenes is highest.26 This information needs to be consistent, particularly in view of the rapidity of information availability and circulation, for example, internet sources including social media. Pregnant women also represent a heterogenous and transient population and therefore food safety advice should be repeated throughout pregnancy.

Thirty percent of participants reported they were yet to receive information from their midwife or lead maternity carer related to food safety. During pregnancy there is a vast amount of information that LMCs are required to share with women and it would be pertinent to consider whether food safety is seen as a priority, and, if not, how this information might be better “packaged” so that it is easier for LMCs to share with their clients.

There was poor adherence related to foods prepared within convenience, take away and restaurant settings. This might reflect confusion about guidance related to these foods, or a lack of adequate education regarding how to manage eating out; an eating pattern that is increasing alongside the increased intakes of ready-to-eat foods.27,28 This should be considered as part of any future review of the guidelines.

An emerging issue related to food safety guidelines is the potential contradiction between safe eating and healthy eating during pregnancy. Obesity in pregnancy is a worsening issue in New Zealand29 and there is conflicting advice regarding eating to support healthy weight gain in pregnancy and eating to avoid listeriosis. For example, a hot meat pie purchased from a shop or café is deemed safe, whereas salads that have been made at a shop or café are not considered safe. Further, there is potentially some ambiguity around foods considered unsafe. For example, salads purchased at a café or restaurant should not be considered unsafe if made freshly with freshly washed ingredients. Poorer diet quality and lower nutrient intakes have been associated with eating according to food safety in pregnancy guidelines.30 There is also potential for confusion and information overload when pregnant women are provided with both the Food Safety in Pregnancy booklet1 and the Ministry of Health’s publication Eating for Healthy Pregnant Women/Ngā Kai Totika Mā Te Wahine Hapu.31 The former emphasises food safety, though makes some reference to healthy eating, and the latter has the opposite emphasis. While these resources could be seen as complementary, there may be merit in considering whether they could be combined.

Conclusion

While the overall average knowledge scores of participants were reassuring, three quarters of participants identified at least one unsafe food as safe to consume in pregnancy. Further, the majority of participants reported continuing to consume foods considered to be unsafe in pregnancy. Māori participants had lower levels of knowledge of food safety in pregnancy and lower adherence to the guidelines. This study highlights the need for comprehensive food safety advice both early in pregnancy and also continued reminders throughout pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Summary

Abstract

Aim

Pregnant women are at increased risk for contracting foodborne illness. Simple food safety precautions can prevent illness. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines.

Method

Participants were recruited when attending antenatal clinics, and via online pregnancy support groups. Knowledge and behaviours were assessed by way of a self-administered questionnaire.

Results

In total, 205 women participated in this study; 100 from antenatal clinics, 105 via Facebook. The median knowledge score was 95% (interquartile range (IQR) 83–100%, minimum = 17.4%). Only 25% of participants answered all questions correctly. The median adherence score was 77% (IQR = 62–92%, minimum = 8%); 13% of participants reported complete adherence to the food safety guidelines. Mean knowledge scores in participants of Māori ethnicity (76.6%) were lower than in participants of European/other ethnicity (91.7%, p=0.004). Māori participants had the lowest mean adherence scores (63.2%) and this requires further investigation.

Conclusion

The majority of participants reported continuing to consume foods considered unsafe in pregnancy. This study highlights the need for improved food safety education during pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Author Information

Emma Jeffs, House Officer, Department of Paediatrics, Christchurch School of Medicine, University of Otago, Christchurch; Jonathan Williman, Biostatistician and Research Fellow, Department of Population Health, University of Otago, Christchurch; Cheryl Brunton, Senior Lecturer, Department of Population Health, University of Otago, Christchurch; Joanna Gullam, Head of Department and Senior Lecturer, Department of Obstetrics and Gynaecology, Christchurch School of Medicine, University of Otago, Christchurch; Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, Christchurch.

Acknowledgements

The authors of this study wish to acknowledge the financial support received from Cure Kids New Zealand. Thank you to Kay Faulls, Professional Practice Fellow/Midwife Tutor, Department of Obstetrics and Gynaecology, University of Otago, Christchurch, for her review of this paper.

Correspondence

Associate Professor Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, PO Box 4345, Christchurch 8140.

Correspondence Email

tony.walls@otago.ac.nz

Competing Interests

Nil.

1. Ministry for Primary Industries. Food safety in pregnancy. Wellington, New Zealand. Available from: http://www.mpi.govt.nz/food-safety/food-safety-for-consumers/food-and-pregnancy/

2. Mateus T, Silva J, Maia RL, Teixeira P. Listeriosis during Pregnancy: A public health concern. ISRN Obstet Gynecol. 2013; 2013:851712.

3. Charlier C, Perrodeau E, Leclercq A, Cazenave B, Pilmis B, Henry B, et al. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. Lancet Infect Dis. 2017; 17(5):510–9.

4. Pattis I, Lopez L, Cressey P, Horn B, Roos R. Annual report concerning foodborne disease in New Zealand 2016. ESR Client Report FW17008. Christchurch, New Zealand; 2017.

5. Elinav H, Hershko-Klement A, Valinsky L, Jaffe J, Wiseman A, Shimon H, et al. Pregnancy-associated listeriosis: clinical characteristics and geospatial analysis of a 10-year period in Israel. Clin Infect Dis. 2014; 59(7):953–61.

6. Infectious disease/CDC update. Vital signs: Listeria illnesses, deaths, and outbreaks - United States, 2009–2011. Ann Emerg Med. 2013; 62(5):536–7.

7. Bryant J, Waller A, Cameron E, Hure A, Sanson-Fisher R. Diet during pregnancy: women’s knowledge of and adherence to food safety guidelines. Aust N Z J Obstet Gynaecol. 2017; 57(3):315–22.

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10. Smith EA, Senter RJ. Automated readability index. AMRL-TR Aerospace Medical Research Laboratories (US). 1967:1–14.

11. Ministry of Health. 2017. HISO 10001:2017 Ethnicity Data Protocols. Wellington: Ministry of Health.

12. Wong LF, Ismail K, Fahy U. Listeria awareness among recently delivered mothers. J Obstet Gynaecol. 2013; 33(8):814–6.

13. Ministry for Primary Industries. Clean, cook, chill 2019. Available from: http://www.mpi.govt.nz/food-safety/food-safety-for-consumers/clean-cook-chill/

14. Kendall P, Scharff R, Baker S, LeJeune J, Sofos J, Medeiros L. Food safety instruction improves knowledge and behavior risk and protection factors for foodborne illnesses in pregnant populations. Matern Child Health J. 2017; 21(8):1686–98.

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Optimal nutrition is important at all stages of life but assumes even greater importance in pregnancy. During pregnancy, nutritional requirements are increased and are critical in supporting the physiological adaptations that occur during pregnancy. In the absence of adequate nutrition, both fetal and maternal health can be adversely affected.

Due to the modulation of the immune system during pregnancy, pregnant women are more susceptible to foodborne illness. Thus, while the intake of adequate nutrients during pregnancy is imperative, so too is ensuring the avoidance of high-risk foods. The New Zealand Food Safety in Pregnancy guidelines, published by the Ministry for Primary Industries,1 provide a number of recommendations for safe eating in pregnancy. These include avoidance of foods that are high risk for the transmission of foodborne infections, including listeriosis and toxoplasmosis, and safe preparation and handling of foods. Listeriosis, caused by the bacteria Listeria monocytogenes, is of particular concern. L. monocytogenes has a predilection to affect pregnant women and neonates. Pregnant women, in particular, are at an approximately 18 times greater risk for infection than the general population.2 In resource-rich countries, L. monocytogenes has the highest case-fatality rate of any foodborne pathogen.3

Listeriosis in pregnancy encompasses maternal, fetal and neonatal disease. Listeriosis most commonly presents in the third trimester of pregnancy (from 28 weeks)4 and is rarely fatal in the mother, particularly in the absence of coexisting medical conditions.5,6 However, if transmitted to the fetus, infection can lead to miscarriage, pre-term delivery or stillbirth. In a recent study of 107 cases of pregnancy-related listeriosis in France, the rate of transmission of infection from the mother to the fetus was 96%, and major fetal or neonatal complications were observed in 83% of infected mothers.3

In New Zealand, lead maternity carers (LMCs), including midwives, general practitioners and obstetricians, are encouraged to provide written and verbal advice regarding food safety in pregnancy, and to reiterate this to women throughout pregnancy. A recent study in Australia reported that the majority of pregnant women have poor knowledge of food safety in pregnancy guidelines and continue to consume foods that put them at increased risk.7 Previous international studies have consistently shown suboptimal adherence among pregnant women to safe eating in pregnancy recommendations.8,9

Pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines, which differ from international guidelines to include foods appropriate for the typical New Zealand diet, has not been studied systematically. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines. Understanding knowledge and behaviour is important to inform the provision of antenatal care and to identify women who are at increased risk and may therefore benefit from more intensive advice and support during pregnancy.

Methods

This cross-sectional study of pregnant women in New Zealand, aimed to examine pregnant women’s knowledge of listeriosis and the New Zealand Food Safety in Pregnancy guidelines and associated eating behaviours.

Questionnaire development

A questionnaire was developed comprising of four broad sections: demographic data, knowledge of the Food Safety in Pregnancy guidelines, behaviours related to safe eating in pregnancy, and safe food handling practices. The questionnaire consisted of 69 questions and took approximately 15 minutes to complete. The Automated Readability Index (ARI) for the questionnaire was calculated according to the formula: 4.71 (characters/words) + 0.5 (words/sentences) – 21.43. The ARI was 5.2 (readability was deemed appropriate for an eight to nine-year-old).10

In questions related to food safety, participants were asked if they thought it was safe to eat each of 23 different foods in pregnancy. Foods considered included those from the New Zealand Food Safety in Pregnancy guidelines: identical wording to the guidelines was used, safe and unsafe foods were included, and foods were listed in a random order. The options ‘yes’, ‘no’ and ‘I don’t know’ were offered. Answers left blank were considered as missing data. To assess behaviours regarding safe eating, participants were asked if they had eaten a range of foods during their current pregnancy. Foods assessed were the same as those in the Food Safety in Pregnancy guidelines and answers were considered correct if they accorded with the guidelines. The options provided included ‘sometimes/often’, ‘never’ and ‘I don’t know’. Finally, we asked about food handling practices in pregnancy and whether participants’ behaviour was consistent with the recommended behaviours. Options provided included ‘always’, ‘sometimes’, ‘never’ and ‘not applicable’.

Pre-testing

Pre-testing of the questionnaire was completed at Christchurch Women’s Hospital (a tertiary care maternity hospital). Twenty women attending an outpatient appointment with an obstetric physician completed the questionnaire. Following pre-testing, no changes were made to the questionnaire, aside from minor changes to layout. Three obstetric specialists and two midwives were also consulted following pre-testing and no further changes were made.

Recruitment

There were two arms to recruitment. Participants were either recruited when attending antenatal clinics at Christchurch Women’s Hospital (hospital cohort) or via Facebook (online cohort). This study was advertised on Facebook pages that were targeted at pregnant women in New Zealand. The questionnaire was delivered via RedCap, a secure web application for managing online questionnaires. Women completed the questionnaire independently, either on iPads provided by the questionnaire coordinators, or on their cell phone or home computer. A recruitment rate was calculated for the hospital cohort as all women offered the questionnaire were counted. A recruitment rate could not be accurately calculated for the Facebook cohort.

Women were eligible to participate if they were currently pregnant, ≥18 years of age, and had sufficient English language literacy to complete the questionnaire. We asked that women had at least one antenatal appointment (eg, with a general practitioner, midwife or obstetric specialist) prior to participation in the study to allow an opportunity for food safety in pregnancy education (it is recommended food safety advice be provided at the earliest opportunity in pregnancy and therefore it would be expected that after a first appointment there should have been at least some advice provided). Recruitment was completed over 30 days in December 2017 and January 2018.

Statistical analysis

For each food included in this study, the proportion of participants who believed the food was a) safe to eat in pregnancy, or b) should be avoided, was determined. This provided an indication of participant knowledge. To determine adherence to the guidelines, the number of women who a) consumed the food (‘sometimes or often’), or b) never consumed the food, was also determined. This provided an indication of participant adherence to the guidelines.

A discrepancy score was calculated by determining the number of participants who correctly indicated that the food should be avoided in pregnancy yet reported consuming the food ‘sometimes or often’. A discrepancy score was only calculated for the foods that are unsafe to eat during pregnancy.

An overall knowledge score was calculated for each participant based on their knowledge of whether the listed foods were safe to consume. Participants were given a score of one if they responded correctly that a food should be avoided or was safe to eat, or zero if they responded incorrectly or that they did not know if a food was safe. An overall score was calculated by summing all 23 foods listed: a higher score indicates greater knowledge. An overall adherence score was also calculated using the same method, but only including the foods that are unsafe to eat during pregnancy (maximum score 13). Knowledge and adherence scores were converted to percentages by dividing overall scores by the number of questions answered. Participant’s missing more than two knowledge or adherence questions were excluded from the analysis. Multivariable linear regression models were used to investigate the characteristics associated with higher levels of knowledge and adherence. Participant ethnicity was based on self-report and prioritised according to New Zealand Ministry of Health guidelines.11

Māori consultation and ethics approval

Māori consultation was sought at the commencement of this project with a University of Otago Kaitohutohu Rangahau/Māori research advisor. This study was approved by the University of Otago Human Ethics Committee (Health), ethics reference number H17/143.

Results

Demographic characteristics of participants

In total, 205 women participated in this study; 100 from the hospital cohort and 105 from the online cohort. The recruitment rate for the hospital cohort was 98.0% (105/107). The characteristics of participants are presented in Table 1.

Table 1: Participant characteristics.

a Predominantly NZ European but also includes European, Middle Eastern, Latin American, and African.
b Locality breakdown not available.
c Includes Samoan, Cook Island Māori, Tongan and Niuean.
d Includes Indian.

The majority of participants were of European/Other ethnicity (74.5%), university educated (71.1%) and in their third trimester of pregnancy (53.2%). Nearly half (47.5%) of participants were primiparous. The median age of participants was 30 years (range 18.7–54.1 years).

Education about the Food Safety in Pregnancy guidelines

Participants reported most commonly receiving food safety advice from their midwife (n=144, 70.2%), family members (n=82, 40.0%), friends (n=81, 39.5%) or their general practitioner (n=67, 32.7%). The majority of participants (n=128, 62.4%) reported completing independent research (eg, on the internet or in books). Nearly three-quarters of participants 146 (71.2%) reported obtaining a copy of the New Zealand Food Safety in Pregnancy guidelines during their current pregnancy, of whom 126 (86.3%) reported reading them.

Concern regarding food safety and reasons to follow the Food Safety in Pregnancy guidelines

Over half of participants (60.0%) reported being ‘very concerned’ (12.7%) or ‘concerned’ (47.3%) about food safety in pregnancy, while 19.5% stated they were ‘neither concerned or not concerned’ and 20.0% stated they were ‘not concerned’. Participants who stated they were ‘very concerned’ or ‘concerned’ were most likely to be in their first (48.7%) or second (32.5%) pregnancy.

The majority of participants agreed that eating according to the Food Safety in Pregnancy guidelines supports maternal health (70.7%) and the health of baby (98.0%). Thirty-three participants (16.1%) also indicated that eating safe foods in pregnancy supports family health.

Knowledge and consumption of unsafe foods during pregnancy

Participant knowledge of the food safety guidelines is presented in Table 2. The most commonly incorrectly identified unsafe foods were cakes, slices and muffins that have added cream or custard (25.5%), hummus (20.6%), salads, including fruit salads, that have been made at a shop or café (18.2%) and cheese that is soft or semi-soft (15.1%).

Table 2: Participant knowledge of the Food Safety in Pregnancy guidelines and their behaviours related to the guidelines.

The most commonly reported unsafe foods consumed in participants’ current pregnancies included cheese that is soft or semi-soft (51.5%), salads, including fruit salads, that have been made at a shop or café (48.3%), dressings served at a restaurant or café, eg, mayonnaise, hollandaise (39.5%), cakes, slices and muffins that have added cream or custard (36.1%), and cold ham or other pre-cooked meat, like chicken and salami (34.2%).

A total knowledge score was calculated for each participant (Table 3). The median knowledge score was 95% (interquartile range [IQR] 83–100%). Only 25% (n=51) of participants answered all questions correctly. Higher average standardised knowledge scores were associated with having a higher level of education (p=0.003) and being of European/Other ethnicity (p=0.0062).

Table 3: Demographic and pregnancy-related factors associated with pregnant women’s knowledge of unsafe foods during pregnancy (knowledge score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised knowledge scores.

The median adherence score was 77% (Table 4; IQR=62–92%, range 7.7–100%). Only 12.9% of participants reported full adherence to the Food Safety in Pregnancy guidelines. Higher average adherence scores were associated lower parity (p=0.002) and having reviewed the Food Safety in Pregnancy guidelines (p=0.007).

Table 4: Demographic and pregnancy-related factors associated with pregnant women’s behaviours related to the Food Safety in Pregnancy guidelines (adherence score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised adherence scores.

Adherence to advice regarding safe food handling in pregnancy is detailed in Table 5. Only 20.1% of participants reported routinely cooking meats until steaming hot and 29.8% of participants reported that they never cook meats until steaming hot. Highest adherence was seen for washing surfaces, utensils and hands after handling raw meat and eggs (89.7%).

Table 5: Participants’ adherence to recommended safe food handling practices in pregnancy.

Discussion

This study identifies considerable gaps in pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines and incomplete adherence to this advice. The New Zealand Food Safety in Pregnancy guidelines are readily available to pregnant women in New Zealand, both online and in print, and have been for at least the past 12 years.

While it is encouraging to note that the average knowledge score across all participants was 95%, only 25% of participants answered all questions correctly, meaning three-quarters of participants incorrectly identified at least one unsafe food as safe to eat in pregnancy. Participants were more certain about ready-to-eat seafood and meats, raw eggs and unpasteurised milk, but were less certain about hummus and cream/custard. Variability in knowledge by food type is an expected finding12 and might reflect knowledge of food safety in general, as well as in pregnancy. For example, raw or undercooked meat and seafoods are known sources of several foodborne illnesses that have been the focus of public health campaigns in New Zealand.13

Knowledge is important, but it is behaviour that ultimately determines risk. Only 13% of participants reported complete adherence to the food safety in pregnancy guidelines. That there is often a poor correlation between knowledge and behaviour with regard to food safety has been reported several times previously.14–16 It is interesting to note the varied levels of compliance around raw seafood versus cold, pre-cooked meat and also the high level of consumption of store bought salads and soft and semi soft cheeses. Adherence to safe food handling behaviours was low overall. Only 20% of participants reported routinely cooking meats until steaming hot. Food handling and preparation are largely unconscious and routine behaviours and achieving behaviour change is known to be problematic in this context.17

In New Zealand, the overall risk of acquiring listeriosis is low. A recent study reported that in the 20-year period from 1997 to 2016 there were 147 cases of listeriosis in women and children that resulted in notification or hospitalisation.18 This study also reported that there had been little change in incidence over time. Despite this, during the period 1 January 2009 to 31 December 2018, L. monocytogenes was associated with the highest number of food recalls due to microbial contamination in Australia (who have a similar food environment to New Zealand). The commonest recalls were for meat (125 recalls), dairy (18 recalls) and processed foods (10 recalls).19 These are food groups for which participants reported poor adherence to the guidelines, both in terms of food intake and food safety-related behaviours. The available New Zealand data (http://www.mpi.govt.nz/food-safety/food-recalls/recalled-food-products) show a similar pattern, although contamination with L. monocytogenes is a less common reason for recall; just four out of 41 recalls in 2019 to mid-September, and none at all in 2018.

There are several reasons why food safety knowledge and adherence might not be optimal. Only 70% of participants reported receiving information from their midwife; 40% received advice from family or friends, and 33% received education from their GP. Further, 62% reported doing their own research. Healthcare providers have previously been identified as the preferred source of food safety advice.20,21 However, there might be inconsistencies in the messages being communicated, or difficulties in comprehension of information. Further contributors might include a lack of recall secondary to information overload in the antenatal period, underestimating risk due to a lack of experience with previous food-related illness, the convenience of high-risk foods overriding food safety advice, and balancing the need for a healthy diet versus the risk for listeriosis. From the perspective of providers of antenatal care, issues such as time constraints, insufficient22 or dated knowledge, or reliance on anecdotal evidence might be contributors.

While it is reported that those of a lower education level are more likely to engage with more risk-taking health behaviours, the same is also true for those of a higher education level. The empirical relationship between education and risk aversion appears ‘U-shaped’, where those with moderate amounts of schooling are the most risk averse.23 It is possible, therefore, that those in our study, who were overall well-educated, were making decisions regarding their own risk assessments, even if aware of the guidance. Other pregnancy-specific changes that might impact eating in pregnancy include food aversion, nausea and emotional eating.

Māori participants had lower reported knowledge of the food safety guidelines and also lower adherence to the guidelines. There are numerous reasons that this might be the case. Firstly, food safety guidance might not adequately reflect eating patterns or behaviours of Māori, for example a higher emphasis on communal food consumption.24 Lower levels of knowledge among those from higher risk groups has been reported previously.2 Health education resources need not only to consider the information they contain but also the way in which it is presented. For example, the current Food Safety in Pregnancy booklet1 features imagery of apparently Pākeha women and a pregnant woman eating alone. It is imperative detailed cultural consultation is included in future revisions of the guidelines.

Strengths and limitations

This study included women across a wide range of the community, including women with higher-risk pregnancies (members of the hospital cohort) and those participating in differing models of obstetric care (those under community midwives only versus those with the addition of specialist obstetric care, including obstetrician oversight, dietetic care and specialist midwifery care). The hospital cohort had a high recruitment rate of 98%.

All data were self-reported, and hence are liable to be affected by social desirability bias. For example, women may have reported not consuming particular foods if they knew that these foods should be avoided in pregnancy. However, participants’ responses were anonymous and were not collected by their obstetric healthcare providers so this might have reduced the impact of this source of bias.

Our sample had a higher proportion of participants with a university education than the general population (71.1% compared to 29.8% for the general population).25 In view of the lower average knowledge scores in participants with lower levels of education, the over-representation of women with a university-level education might mean that our study provides an overestimate of knowledge related to the New Zealand Food Safety in Pregnancy guidelines, and actual knowledge levels might be lower than we have found. We only included participants who self-identified as having adequate English language literacy to complete the questionnaire; this might limit the findings in those of ethnic minorities. Our sample had lower numbers of Māori and Pacific participants when compared to the general population of New Zealand.

Implications

The findings of this study indicate that the majority of participants did not have complete knowledge of the New Zealand Food Safety in Pregnancy guidelines. Provision of information regarding high-risk foods and high-risk behaviours related to the safe handling of food should ideally take place at the first antenatal appointment when the threat to fetal health due to L. monocytogenes is highest.26 This information needs to be consistent, particularly in view of the rapidity of information availability and circulation, for example, internet sources including social media. Pregnant women also represent a heterogenous and transient population and therefore food safety advice should be repeated throughout pregnancy.

Thirty percent of participants reported they were yet to receive information from their midwife or lead maternity carer related to food safety. During pregnancy there is a vast amount of information that LMCs are required to share with women and it would be pertinent to consider whether food safety is seen as a priority, and, if not, how this information might be better “packaged” so that it is easier for LMCs to share with their clients.

There was poor adherence related to foods prepared within convenience, take away and restaurant settings. This might reflect confusion about guidance related to these foods, or a lack of adequate education regarding how to manage eating out; an eating pattern that is increasing alongside the increased intakes of ready-to-eat foods.27,28 This should be considered as part of any future review of the guidelines.

An emerging issue related to food safety guidelines is the potential contradiction between safe eating and healthy eating during pregnancy. Obesity in pregnancy is a worsening issue in New Zealand29 and there is conflicting advice regarding eating to support healthy weight gain in pregnancy and eating to avoid listeriosis. For example, a hot meat pie purchased from a shop or café is deemed safe, whereas salads that have been made at a shop or café are not considered safe. Further, there is potentially some ambiguity around foods considered unsafe. For example, salads purchased at a café or restaurant should not be considered unsafe if made freshly with freshly washed ingredients. Poorer diet quality and lower nutrient intakes have been associated with eating according to food safety in pregnancy guidelines.30 There is also potential for confusion and information overload when pregnant women are provided with both the Food Safety in Pregnancy booklet1 and the Ministry of Health’s publication Eating for Healthy Pregnant Women/Ngā Kai Totika Mā Te Wahine Hapu.31 The former emphasises food safety, though makes some reference to healthy eating, and the latter has the opposite emphasis. While these resources could be seen as complementary, there may be merit in considering whether they could be combined.

Conclusion

While the overall average knowledge scores of participants were reassuring, three quarters of participants identified at least one unsafe food as safe to consume in pregnancy. Further, the majority of participants reported continuing to consume foods considered to be unsafe in pregnancy. Māori participants had lower levels of knowledge of food safety in pregnancy and lower adherence to the guidelines. This study highlights the need for comprehensive food safety advice both early in pregnancy and also continued reminders throughout pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Summary

Abstract

Aim

Pregnant women are at increased risk for contracting foodborne illness. Simple food safety precautions can prevent illness. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines.

Method

Participants were recruited when attending antenatal clinics, and via online pregnancy support groups. Knowledge and behaviours were assessed by way of a self-administered questionnaire.

Results

In total, 205 women participated in this study; 100 from antenatal clinics, 105 via Facebook. The median knowledge score was 95% (interquartile range (IQR) 83–100%, minimum = 17.4%). Only 25% of participants answered all questions correctly. The median adherence score was 77% (IQR = 62–92%, minimum = 8%); 13% of participants reported complete adherence to the food safety guidelines. Mean knowledge scores in participants of Māori ethnicity (76.6%) were lower than in participants of European/other ethnicity (91.7%, p=0.004). Māori participants had the lowest mean adherence scores (63.2%) and this requires further investigation.

Conclusion

The majority of participants reported continuing to consume foods considered unsafe in pregnancy. This study highlights the need for improved food safety education during pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Author Information

Emma Jeffs, House Officer, Department of Paediatrics, Christchurch School of Medicine, University of Otago, Christchurch; Jonathan Williman, Biostatistician and Research Fellow, Department of Population Health, University of Otago, Christchurch; Cheryl Brunton, Senior Lecturer, Department of Population Health, University of Otago, Christchurch; Joanna Gullam, Head of Department and Senior Lecturer, Department of Obstetrics and Gynaecology, Christchurch School of Medicine, University of Otago, Christchurch; Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, Christchurch.

Acknowledgements

The authors of this study wish to acknowledge the financial support received from Cure Kids New Zealand. Thank you to Kay Faulls, Professional Practice Fellow/Midwife Tutor, Department of Obstetrics and Gynaecology, University of Otago, Christchurch, for her review of this paper.

Correspondence

Associate Professor Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, PO Box 4345, Christchurch 8140.

Correspondence Email

tony.walls@otago.ac.nz

Competing Interests

Nil.

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Optimal nutrition is important at all stages of life but assumes even greater importance in pregnancy. During pregnancy, nutritional requirements are increased and are critical in supporting the physiological adaptations that occur during pregnancy. In the absence of adequate nutrition, both fetal and maternal health can be adversely affected.

Due to the modulation of the immune system during pregnancy, pregnant women are more susceptible to foodborne illness. Thus, while the intake of adequate nutrients during pregnancy is imperative, so too is ensuring the avoidance of high-risk foods. The New Zealand Food Safety in Pregnancy guidelines, published by the Ministry for Primary Industries,1 provide a number of recommendations for safe eating in pregnancy. These include avoidance of foods that are high risk for the transmission of foodborne infections, including listeriosis and toxoplasmosis, and safe preparation and handling of foods. Listeriosis, caused by the bacteria Listeria monocytogenes, is of particular concern. L. monocytogenes has a predilection to affect pregnant women and neonates. Pregnant women, in particular, are at an approximately 18 times greater risk for infection than the general population.2 In resource-rich countries, L. monocytogenes has the highest case-fatality rate of any foodborne pathogen.3

Listeriosis in pregnancy encompasses maternal, fetal and neonatal disease. Listeriosis most commonly presents in the third trimester of pregnancy (from 28 weeks)4 and is rarely fatal in the mother, particularly in the absence of coexisting medical conditions.5,6 However, if transmitted to the fetus, infection can lead to miscarriage, pre-term delivery or stillbirth. In a recent study of 107 cases of pregnancy-related listeriosis in France, the rate of transmission of infection from the mother to the fetus was 96%, and major fetal or neonatal complications were observed in 83% of infected mothers.3

In New Zealand, lead maternity carers (LMCs), including midwives, general practitioners and obstetricians, are encouraged to provide written and verbal advice regarding food safety in pregnancy, and to reiterate this to women throughout pregnancy. A recent study in Australia reported that the majority of pregnant women have poor knowledge of food safety in pregnancy guidelines and continue to consume foods that put them at increased risk.7 Previous international studies have consistently shown suboptimal adherence among pregnant women to safe eating in pregnancy recommendations.8,9

Pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines, which differ from international guidelines to include foods appropriate for the typical New Zealand diet, has not been studied systematically. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines. Understanding knowledge and behaviour is important to inform the provision of antenatal care and to identify women who are at increased risk and may therefore benefit from more intensive advice and support during pregnancy.

Methods

This cross-sectional study of pregnant women in New Zealand, aimed to examine pregnant women’s knowledge of listeriosis and the New Zealand Food Safety in Pregnancy guidelines and associated eating behaviours.

Questionnaire development

A questionnaire was developed comprising of four broad sections: demographic data, knowledge of the Food Safety in Pregnancy guidelines, behaviours related to safe eating in pregnancy, and safe food handling practices. The questionnaire consisted of 69 questions and took approximately 15 minutes to complete. The Automated Readability Index (ARI) for the questionnaire was calculated according to the formula: 4.71 (characters/words) + 0.5 (words/sentences) – 21.43. The ARI was 5.2 (readability was deemed appropriate for an eight to nine-year-old).10

In questions related to food safety, participants were asked if they thought it was safe to eat each of 23 different foods in pregnancy. Foods considered included those from the New Zealand Food Safety in Pregnancy guidelines: identical wording to the guidelines was used, safe and unsafe foods were included, and foods were listed in a random order. The options ‘yes’, ‘no’ and ‘I don’t know’ were offered. Answers left blank were considered as missing data. To assess behaviours regarding safe eating, participants were asked if they had eaten a range of foods during their current pregnancy. Foods assessed were the same as those in the Food Safety in Pregnancy guidelines and answers were considered correct if they accorded with the guidelines. The options provided included ‘sometimes/often’, ‘never’ and ‘I don’t know’. Finally, we asked about food handling practices in pregnancy and whether participants’ behaviour was consistent with the recommended behaviours. Options provided included ‘always’, ‘sometimes’, ‘never’ and ‘not applicable’.

Pre-testing

Pre-testing of the questionnaire was completed at Christchurch Women’s Hospital (a tertiary care maternity hospital). Twenty women attending an outpatient appointment with an obstetric physician completed the questionnaire. Following pre-testing, no changes were made to the questionnaire, aside from minor changes to layout. Three obstetric specialists and two midwives were also consulted following pre-testing and no further changes were made.

Recruitment

There were two arms to recruitment. Participants were either recruited when attending antenatal clinics at Christchurch Women’s Hospital (hospital cohort) or via Facebook (online cohort). This study was advertised on Facebook pages that were targeted at pregnant women in New Zealand. The questionnaire was delivered via RedCap, a secure web application for managing online questionnaires. Women completed the questionnaire independently, either on iPads provided by the questionnaire coordinators, or on their cell phone or home computer. A recruitment rate was calculated for the hospital cohort as all women offered the questionnaire were counted. A recruitment rate could not be accurately calculated for the Facebook cohort.

Women were eligible to participate if they were currently pregnant, ≥18 years of age, and had sufficient English language literacy to complete the questionnaire. We asked that women had at least one antenatal appointment (eg, with a general practitioner, midwife or obstetric specialist) prior to participation in the study to allow an opportunity for food safety in pregnancy education (it is recommended food safety advice be provided at the earliest opportunity in pregnancy and therefore it would be expected that after a first appointment there should have been at least some advice provided). Recruitment was completed over 30 days in December 2017 and January 2018.

Statistical analysis

For each food included in this study, the proportion of participants who believed the food was a) safe to eat in pregnancy, or b) should be avoided, was determined. This provided an indication of participant knowledge. To determine adherence to the guidelines, the number of women who a) consumed the food (‘sometimes or often’), or b) never consumed the food, was also determined. This provided an indication of participant adherence to the guidelines.

A discrepancy score was calculated by determining the number of participants who correctly indicated that the food should be avoided in pregnancy yet reported consuming the food ‘sometimes or often’. A discrepancy score was only calculated for the foods that are unsafe to eat during pregnancy.

An overall knowledge score was calculated for each participant based on their knowledge of whether the listed foods were safe to consume. Participants were given a score of one if they responded correctly that a food should be avoided or was safe to eat, or zero if they responded incorrectly or that they did not know if a food was safe. An overall score was calculated by summing all 23 foods listed: a higher score indicates greater knowledge. An overall adherence score was also calculated using the same method, but only including the foods that are unsafe to eat during pregnancy (maximum score 13). Knowledge and adherence scores were converted to percentages by dividing overall scores by the number of questions answered. Participant’s missing more than two knowledge or adherence questions were excluded from the analysis. Multivariable linear regression models were used to investigate the characteristics associated with higher levels of knowledge and adherence. Participant ethnicity was based on self-report and prioritised according to New Zealand Ministry of Health guidelines.11

Māori consultation and ethics approval

Māori consultation was sought at the commencement of this project with a University of Otago Kaitohutohu Rangahau/Māori research advisor. This study was approved by the University of Otago Human Ethics Committee (Health), ethics reference number H17/143.

Results

Demographic characteristics of participants

In total, 205 women participated in this study; 100 from the hospital cohort and 105 from the online cohort. The recruitment rate for the hospital cohort was 98.0% (105/107). The characteristics of participants are presented in Table 1.

Table 1: Participant characteristics.

a Predominantly NZ European but also includes European, Middle Eastern, Latin American, and African.
b Locality breakdown not available.
c Includes Samoan, Cook Island Māori, Tongan and Niuean.
d Includes Indian.

The majority of participants were of European/Other ethnicity (74.5%), university educated (71.1%) and in their third trimester of pregnancy (53.2%). Nearly half (47.5%) of participants were primiparous. The median age of participants was 30 years (range 18.7–54.1 years).

Education about the Food Safety in Pregnancy guidelines

Participants reported most commonly receiving food safety advice from their midwife (n=144, 70.2%), family members (n=82, 40.0%), friends (n=81, 39.5%) or their general practitioner (n=67, 32.7%). The majority of participants (n=128, 62.4%) reported completing independent research (eg, on the internet or in books). Nearly three-quarters of participants 146 (71.2%) reported obtaining a copy of the New Zealand Food Safety in Pregnancy guidelines during their current pregnancy, of whom 126 (86.3%) reported reading them.

Concern regarding food safety and reasons to follow the Food Safety in Pregnancy guidelines

Over half of participants (60.0%) reported being ‘very concerned’ (12.7%) or ‘concerned’ (47.3%) about food safety in pregnancy, while 19.5% stated they were ‘neither concerned or not concerned’ and 20.0% stated they were ‘not concerned’. Participants who stated they were ‘very concerned’ or ‘concerned’ were most likely to be in their first (48.7%) or second (32.5%) pregnancy.

The majority of participants agreed that eating according to the Food Safety in Pregnancy guidelines supports maternal health (70.7%) and the health of baby (98.0%). Thirty-three participants (16.1%) also indicated that eating safe foods in pregnancy supports family health.

Knowledge and consumption of unsafe foods during pregnancy

Participant knowledge of the food safety guidelines is presented in Table 2. The most commonly incorrectly identified unsafe foods were cakes, slices and muffins that have added cream or custard (25.5%), hummus (20.6%), salads, including fruit salads, that have been made at a shop or café (18.2%) and cheese that is soft or semi-soft (15.1%).

Table 2: Participant knowledge of the Food Safety in Pregnancy guidelines and their behaviours related to the guidelines.

The most commonly reported unsafe foods consumed in participants’ current pregnancies included cheese that is soft or semi-soft (51.5%), salads, including fruit salads, that have been made at a shop or café (48.3%), dressings served at a restaurant or café, eg, mayonnaise, hollandaise (39.5%), cakes, slices and muffins that have added cream or custard (36.1%), and cold ham or other pre-cooked meat, like chicken and salami (34.2%).

A total knowledge score was calculated for each participant (Table 3). The median knowledge score was 95% (interquartile range [IQR] 83–100%). Only 25% (n=51) of participants answered all questions correctly. Higher average standardised knowledge scores were associated with having a higher level of education (p=0.003) and being of European/Other ethnicity (p=0.0062).

Table 3: Demographic and pregnancy-related factors associated with pregnant women’s knowledge of unsafe foods during pregnancy (knowledge score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised knowledge scores.

The median adherence score was 77% (Table 4; IQR=62–92%, range 7.7–100%). Only 12.9% of participants reported full adherence to the Food Safety in Pregnancy guidelines. Higher average adherence scores were associated lower parity (p=0.002) and having reviewed the Food Safety in Pregnancy guidelines (p=0.007).

Table 4: Demographic and pregnancy-related factors associated with pregnant women’s behaviours related to the Food Safety in Pregnancy guidelines (adherence score).

a Participants who responded ‘I don’t know’ or who did not respond were excluded from analysis.
b Coefficients are calculated from a multivariable adjusted linear model and represent estimated differences in mean standardised adherence scores.

Adherence to advice regarding safe food handling in pregnancy is detailed in Table 5. Only 20.1% of participants reported routinely cooking meats until steaming hot and 29.8% of participants reported that they never cook meats until steaming hot. Highest adherence was seen for washing surfaces, utensils and hands after handling raw meat and eggs (89.7%).

Table 5: Participants’ adherence to recommended safe food handling practices in pregnancy.

Discussion

This study identifies considerable gaps in pregnant women’s knowledge of the New Zealand Food Safety in Pregnancy guidelines and incomplete adherence to this advice. The New Zealand Food Safety in Pregnancy guidelines are readily available to pregnant women in New Zealand, both online and in print, and have been for at least the past 12 years.

While it is encouraging to note that the average knowledge score across all participants was 95%, only 25% of participants answered all questions correctly, meaning three-quarters of participants incorrectly identified at least one unsafe food as safe to eat in pregnancy. Participants were more certain about ready-to-eat seafood and meats, raw eggs and unpasteurised milk, but were less certain about hummus and cream/custard. Variability in knowledge by food type is an expected finding12 and might reflect knowledge of food safety in general, as well as in pregnancy. For example, raw or undercooked meat and seafoods are known sources of several foodborne illnesses that have been the focus of public health campaigns in New Zealand.13

Knowledge is important, but it is behaviour that ultimately determines risk. Only 13% of participants reported complete adherence to the food safety in pregnancy guidelines. That there is often a poor correlation between knowledge and behaviour with regard to food safety has been reported several times previously.14–16 It is interesting to note the varied levels of compliance around raw seafood versus cold, pre-cooked meat and also the high level of consumption of store bought salads and soft and semi soft cheeses. Adherence to safe food handling behaviours was low overall. Only 20% of participants reported routinely cooking meats until steaming hot. Food handling and preparation are largely unconscious and routine behaviours and achieving behaviour change is known to be problematic in this context.17

In New Zealand, the overall risk of acquiring listeriosis is low. A recent study reported that in the 20-year period from 1997 to 2016 there were 147 cases of listeriosis in women and children that resulted in notification or hospitalisation.18 This study also reported that there had been little change in incidence over time. Despite this, during the period 1 January 2009 to 31 December 2018, L. monocytogenes was associated with the highest number of food recalls due to microbial contamination in Australia (who have a similar food environment to New Zealand). The commonest recalls were for meat (125 recalls), dairy (18 recalls) and processed foods (10 recalls).19 These are food groups for which participants reported poor adherence to the guidelines, both in terms of food intake and food safety-related behaviours. The available New Zealand data (http://www.mpi.govt.nz/food-safety/food-recalls/recalled-food-products) show a similar pattern, although contamination with L. monocytogenes is a less common reason for recall; just four out of 41 recalls in 2019 to mid-September, and none at all in 2018.

There are several reasons why food safety knowledge and adherence might not be optimal. Only 70% of participants reported receiving information from their midwife; 40% received advice from family or friends, and 33% received education from their GP. Further, 62% reported doing their own research. Healthcare providers have previously been identified as the preferred source of food safety advice.20,21 However, there might be inconsistencies in the messages being communicated, or difficulties in comprehension of information. Further contributors might include a lack of recall secondary to information overload in the antenatal period, underestimating risk due to a lack of experience with previous food-related illness, the convenience of high-risk foods overriding food safety advice, and balancing the need for a healthy diet versus the risk for listeriosis. From the perspective of providers of antenatal care, issues such as time constraints, insufficient22 or dated knowledge, or reliance on anecdotal evidence might be contributors.

While it is reported that those of a lower education level are more likely to engage with more risk-taking health behaviours, the same is also true for those of a higher education level. The empirical relationship between education and risk aversion appears ‘U-shaped’, where those with moderate amounts of schooling are the most risk averse.23 It is possible, therefore, that those in our study, who were overall well-educated, were making decisions regarding their own risk assessments, even if aware of the guidance. Other pregnancy-specific changes that might impact eating in pregnancy include food aversion, nausea and emotional eating.

Māori participants had lower reported knowledge of the food safety guidelines and also lower adherence to the guidelines. There are numerous reasons that this might be the case. Firstly, food safety guidance might not adequately reflect eating patterns or behaviours of Māori, for example a higher emphasis on communal food consumption.24 Lower levels of knowledge among those from higher risk groups has been reported previously.2 Health education resources need not only to consider the information they contain but also the way in which it is presented. For example, the current Food Safety in Pregnancy booklet1 features imagery of apparently Pākeha women and a pregnant woman eating alone. It is imperative detailed cultural consultation is included in future revisions of the guidelines.

Strengths and limitations

This study included women across a wide range of the community, including women with higher-risk pregnancies (members of the hospital cohort) and those participating in differing models of obstetric care (those under community midwives only versus those with the addition of specialist obstetric care, including obstetrician oversight, dietetic care and specialist midwifery care). The hospital cohort had a high recruitment rate of 98%.

All data were self-reported, and hence are liable to be affected by social desirability bias. For example, women may have reported not consuming particular foods if they knew that these foods should be avoided in pregnancy. However, participants’ responses were anonymous and were not collected by their obstetric healthcare providers so this might have reduced the impact of this source of bias.

Our sample had a higher proportion of participants with a university education than the general population (71.1% compared to 29.8% for the general population).25 In view of the lower average knowledge scores in participants with lower levels of education, the over-representation of women with a university-level education might mean that our study provides an overestimate of knowledge related to the New Zealand Food Safety in Pregnancy guidelines, and actual knowledge levels might be lower than we have found. We only included participants who self-identified as having adequate English language literacy to complete the questionnaire; this might limit the findings in those of ethnic minorities. Our sample had lower numbers of Māori and Pacific participants when compared to the general population of New Zealand.

Implications

The findings of this study indicate that the majority of participants did not have complete knowledge of the New Zealand Food Safety in Pregnancy guidelines. Provision of information regarding high-risk foods and high-risk behaviours related to the safe handling of food should ideally take place at the first antenatal appointment when the threat to fetal health due to L. monocytogenes is highest.26 This information needs to be consistent, particularly in view of the rapidity of information availability and circulation, for example, internet sources including social media. Pregnant women also represent a heterogenous and transient population and therefore food safety advice should be repeated throughout pregnancy.

Thirty percent of participants reported they were yet to receive information from their midwife or lead maternity carer related to food safety. During pregnancy there is a vast amount of information that LMCs are required to share with women and it would be pertinent to consider whether food safety is seen as a priority, and, if not, how this information might be better “packaged” so that it is easier for LMCs to share with their clients.

There was poor adherence related to foods prepared within convenience, take away and restaurant settings. This might reflect confusion about guidance related to these foods, or a lack of adequate education regarding how to manage eating out; an eating pattern that is increasing alongside the increased intakes of ready-to-eat foods.27,28 This should be considered as part of any future review of the guidelines.

An emerging issue related to food safety guidelines is the potential contradiction between safe eating and healthy eating during pregnancy. Obesity in pregnancy is a worsening issue in New Zealand29 and there is conflicting advice regarding eating to support healthy weight gain in pregnancy and eating to avoid listeriosis. For example, a hot meat pie purchased from a shop or café is deemed safe, whereas salads that have been made at a shop or café are not considered safe. Further, there is potentially some ambiguity around foods considered unsafe. For example, salads purchased at a café or restaurant should not be considered unsafe if made freshly with freshly washed ingredients. Poorer diet quality and lower nutrient intakes have been associated with eating according to food safety in pregnancy guidelines.30 There is also potential for confusion and information overload when pregnant women are provided with both the Food Safety in Pregnancy booklet1 and the Ministry of Health’s publication Eating for Healthy Pregnant Women/Ngā Kai Totika Mā Te Wahine Hapu.31 The former emphasises food safety, though makes some reference to healthy eating, and the latter has the opposite emphasis. While these resources could be seen as complementary, there may be merit in considering whether they could be combined.

Conclusion

While the overall average knowledge scores of participants were reassuring, three quarters of participants identified at least one unsafe food as safe to consume in pregnancy. Further, the majority of participants reported continuing to consume foods considered to be unsafe in pregnancy. Māori participants had lower levels of knowledge of food safety in pregnancy and lower adherence to the guidelines. This study highlights the need for comprehensive food safety advice both early in pregnancy and also continued reminders throughout pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Summary

Abstract

Aim

Pregnant women are at increased risk for contracting foodborne illness. Simple food safety precautions can prevent illness. The aim of this study was to examine pregnant women’s knowledge of, and adherence to, the New Zealand Food Safety in Pregnancy guidelines.

Method

Participants were recruited when attending antenatal clinics, and via online pregnancy support groups. Knowledge and behaviours were assessed by way of a self-administered questionnaire.

Results

In total, 205 women participated in this study; 100 from antenatal clinics, 105 via Facebook. The median knowledge score was 95% (interquartile range (IQR) 83–100%, minimum = 17.4%). Only 25% of participants answered all questions correctly. The median adherence score was 77% (IQR = 62–92%, minimum = 8%); 13% of participants reported complete adherence to the food safety guidelines. Mean knowledge scores in participants of Māori ethnicity (76.6%) were lower than in participants of European/other ethnicity (91.7%, p=0.004). Māori participants had the lowest mean adherence scores (63.2%) and this requires further investigation.

Conclusion

The majority of participants reported continuing to consume foods considered unsafe in pregnancy. This study highlights the need for improved food safety education during pregnancy. The results also suggest a need for food safety guidance to be made more accessible and relevant to the needs of Māori women.

Author Information

Emma Jeffs, House Officer, Department of Paediatrics, Christchurch School of Medicine, University of Otago, Christchurch; Jonathan Williman, Biostatistician and Research Fellow, Department of Population Health, University of Otago, Christchurch; Cheryl Brunton, Senior Lecturer, Department of Population Health, University of Otago, Christchurch; Joanna Gullam, Head of Department and Senior Lecturer, Department of Obstetrics and Gynaecology, Christchurch School of Medicine, University of Otago, Christchurch; Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, Christchurch.

Acknowledgements

The authors of this study wish to acknowledge the financial support received from Cure Kids New Zealand. Thank you to Kay Faulls, Professional Practice Fellow/Midwife Tutor, Department of Obstetrics and Gynaecology, University of Otago, Christchurch, for her review of this paper.

Correspondence

Associate Professor Tony Walls, Infectious Diseases Specialist and Consultant Paediatrician, University of Otago, PO Box 4345, Christchurch 8140.

Correspondence Email

tony.walls@otago.ac.nz

Competing Interests

Nil.

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