Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies
BMJ 2019; 367 doi: https://doi.org/10.1136/bmj.l6204 (Published 27 November 2019) Cite this as: BMJ 2019;367:l6204
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The consumption of dairy products has been shown to have health benefits for general populations [1-2], but harms for some chronic conditions e.g. in patients with chronic renal failure [3]. In a study conducted by Ding and colleagues using the data from three prospective cohort studies, the high consumption of dairy foods did not show the inverse association with mortality risk in men and women [4]. However, in a randomized crossover trial, people who consumed a high-dairy diet (5-6 dairy portions per day) as compared with a low-dairy diet (≤1 dairy portion per day) had a significant reduction in both systolic blood pressure and diastolic blood pressure in overweight middle-aged women and men [1]. In another randomized crossover intervention, adults who consumed either high- or low- dairy diet during the 6-week trial had a similar effect on fasting glucose, postprandial glucose and insulin responses, and glucose kinetics [2]. These inconsistencies require more trials to examine the effect of different types of dairy foods in different subgroups.
References
1. Rietsema, S.; Eelderink, C.; Joustra, M.L.; van Vliet, I.M.Y.; van Londen, M.; Corpeleijn, E.; Singh-Povel, C.M.; Geurts, J.M.W.; Kootstra-Ros, J.E.; Westerhuis, R.; et al. Effect of high compared with low dairy intake on blood pressure in overweight middle-aged adults: results of a randomized crossover intervention study. Am. J. Clin. Nutr. 2019, 110, 340–348.
2. Eelderink, C.; Rietsema, S.; van Vliet, I.M.Y.; Loef, L.C.; Boer, T.; Koehorst, M.; Nolte, I.M.; Westerhuis, R.; Singh-Povel, C.M.; Geurts, J.M.W.; et al. The effect of high compared with low dairy consumption on glucose metabolism, insulin sensitivity, and metabolic flexibility in overweight adults: a randomized crossover trial. Am. J. Clin. Nutr. 2019, 109, 1555-1568.
3. K/DOQI Workgroup. K/DOQI Clinical Practice Guidelines for Nutrition in Chronic Renal Failure. Am. J. Kidney Dis. 2000, 35, S1-S140.
4. Ding, M.; Li, J.; Qi, L.; Ellervik, C.; Zhang, X.; Manson, J.E.; Stampfer, M.; Chavarro, J.E.; Rexrode, K.M.; Kraft, P.; et al. Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies. BMJ 2019, 367, l6204.
Competing interests: No competing interests
Dear Editor
I confess that I get lost in the maze of statistics.
Might I request the authors, the rapid responders and indeed others from all parts of the world, to enlighten me on a few points? On the matter of differences in the mammary secretion of various animals.
1. In Europe and the USA, it is almost exclusively the cow. Bos taurus, I believe.
2. There are in England and in Eastern Europe, some herds of Bubalus bubalis. Commonly known as the buffalo. Much commoner in Pakistan and in India.
3. The goat, Capra hircus, supplies some milk in England, a lot in some arid regions of the Middle East.
4. The sheep, Ovis aries, supplies milk in Europe, the Middle East, perhaps elsewhere.
5. The camel (Camelus) of two species - the Dromedary and the Bactrian camel. Its milk is used in North Africa, the Middle East and is now produced on a commercial scale in Australia.
6. The ass (Equus asinus). The milk is said to be close in composition to human milk and more easily digested.
I believe that the milk of all these species differs in chemical composition.
Further, depending on hygienic customs, and on pasteurisation, the milk from these different animals will have different microorganisms in them - and these will colonise the gut of the consumer.
Should we not consider whether the health of the consumers is influenced by the differences in dairy products?
Competing interests: No competing interests
We appreciate Ding et al for the meticulous work done on the study “Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies”1 recently published in The BMJ. However, we wish to draw attention to certain factors of public health significance which we believe could have impacted the results.
It is an undeniable fact that diet is a major contributor to overall health and mortality and certainly the role of milk cannot be overlooked. However, it is also worth noting that foods don’t work in isolation, requiring that certain influencing factors are taking into account in relating any particular food or diet to overall health and mortality. Accumulating evidence demonstrate that breastfeeding in early life is a critical “window of opportunity” that allows for long term impact on the gut microbiota which is now a “hot cake” subject linked to many diseases and mortality including cancer, cardiovascular and many other chronic diseases.2 Interestingly, findings also indicate that the sterile in utero gastrointestinal tract gets its first microbiota colonization through vaginal delivery but not caesarian section (CS) and the colonized bacteria species persist even into aduldhood. Therefore the mode of delivery (vaginal or CS) and subsequent breastfeeding status (breastfed or not breastfed) are important in shaping the gut microbiota. Consequently, it is imperative that studies relating any factors to disease and mortality even in later life account for the mode of delivery and breastfeeding status since these are critical factors that could impact overall health and wellbeing even later in life via gut microbiota programming. We realized that, in the report by Ding et al, like many similar studies already published, this important public health factor was not reported and/or accounted for in the study population and we believe this could have significantly impacted the overall results. We therefore suggest that future study designs account for these.
In addition, the authors grouped dairy products into milk, cheese, yogurt, and other types of dairy foods including ice cream, cream, and sherbert. Even though this model seems common in many epidemiological studies, we are of the view that it does not capture the important factor of the effect of processing technology on milk (especially milk proteins) and health. It is known that treatment technologies like chemical, biochemical, thermal and physical treatments of milk all have varying effects on the quality of milk with attendant changes in antigenicity and health in general. For example, the type and level of heat treatment could significantly impact the digestibility and digestion kinetics of the milk proteins as well as the bioavailability of essential amino acids with potential consequences for immunity. Processing levels could also induce reactions such as Maillard reactions which could generate intermediate products that could be toxic and/or antigenic upon consumption at elevated levels.3 4 Moreover, it has been reported that thermal processing of food significantly reshaped the gut microbial diversity and differentially triggered microbial alterations5 with significant consequences for health, disease and mortality. Therefore in evaluating associations between dairy consumption and disease and / or mortality, dairy types must reflect the processing techniques used as these might better reflect physiological impact.
Furthermore, taking yogurt for example, commercially supplied yogurt products comes in plain or with added fruits, flavor enhancers, coloring agents and other food ingredients (including food additives, either natural or artificial). Added agents and enhancers could potentially counter the beneficial effects of yoghurt, if any. Interestingly, yogurt topped with fruits could supply mixed nutrients and exert combined health benefits through potential prebiotic and probiotic effects.6 Therefore, yogurt topped with different fruits and other agents such as coloring might exert varying influences on the conclusion of such studies and so generalizing the effect of yoghurt consumption without accounting for these may confound the outcome.
In conclusion, dairy consumption would definitely impact health and mortality but certain critical factors that could potentially and significantly impact the direction of such relationship directly or indirectly must be accounted for, especially when previous study results have been inconsistent. This would allow for more robust findings and conclusions to be made.
Conflict of interest: We declare that we have no conflict of interest
References
1. Ding M, Li J, Qi L, et al. Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies. bmj 2019;367
2. Van den Elsen L, Garssen J, Burcelin R, et al. Shaping the gut microbiota by breastfeeding: the gateway to allergy prevention? Frontiers in pediatrics 2019;7:47.
3. van Lieshout GA, Lambers TT, Bragt MC, et al. How processing may affect milk protein digestion and overall physiological outcomes: A systematic review. Critical reviews in food science and nutrition 2019:1-24.
4. Borad SG, Kumar A, Singh AK. Effect of processing on nutritive values of milk protein. Critical reviews in food science and nutrition 2017;57(17):3690-702.
5. Zhang Z, Li D. Thermal processing of food reduces gut microbiota diversity of the host and triggers adaptation of the microbiota: evidence from two vertebrates. Microbiome 2018;6(1) doi: 10.1186/s40168-018-0471-y
6. Fernandez MA, Marette A. Potential health benefits of combining yogurt and fruits based on their probiotic and prebiotic properties. Advances in Nutrition 2017;8(1):155S-64S.
Competing interests: No competing interests
The most significant association in this paper is in table 1.
Low dairy intake is associated with an energy intake of under 1500 calories - high dairy intake is associated with an energy intake of over 2000 calories (in the 2 cohorts of women - the male association is the same with more calories).
Yet there is no difference in BMI between quintiles.
This should have been the headline finding. Does dairy intake allow us to eat an extra 500 calories without weight gain? That would be more important information than the slight difference in mortality, considering all the residual confounding that must be associated with higher vs lower energy intakes.
Competing interests: No competing interests
Ding et al (1) have provided a thorough investigation on the association between dairy consumption and time to death by use of three large well-characterized cohorts within a setting of health professionals in USA. The study is, as expected with this team of authors, carefully done. For the reader it is, however, not easy to interpret these new results in the context of other prior cohort results. We would therefore take the opportunity and ask the authors if they can provide some additional information that would facilitate interpretation of their results. In addition, we would like to make some own remarks and also compare these new results with other cohort studies undertaken within other settings. Specifically, there are substantial differences in exposure range, reference category used and type of exposure.
The main exposure in the study (1) is total dairy consumption, a mixture of different dairy products and the composition of this mixture will depend on the setting. It would be of value if the authors present the relative contribution of different dairy products for the categories of total dairy intake presented in table 1. What were the relative contributions of e.g., non-fermented low-fat milk, high-fat milk, cheese, yogurt, etc? It would also be of interest to see average fruit and vegetable consumption in the categories of dairy, to facilitate comparison with other studies (2).
Reference and exposure categories vary considerably in the analyses (1). For NHS I, the reference averaged 0.7 serving/day of total dairy and highest category 4.1 servings/day. This is substantially different compared with the more restricted exposure width when low-fat milk was analyzed, with less than 1 serving/week as reference and 1.5 serving/day or more as highest category. For high-fat milk/whole milk, the reference was less than one serving/month and highest category 2 servings/week or more. Moreover, it is unclear how the authors treated whole milk consumption when low-fat milk was considered as the exposure, and vice versa. Were whole milk consumers retained in for example the reference category of low-fat milk? In a footnote below Table 3 it is stated that “Subtypes of dairy foods were adjusted for each other” and it is unclear whether the authors by this formulation meant dairy food groups described in the Methods, or mutual adjustment for the dairy products used as exposures in Table 3. Nevertheless, an adjustment does not remove the problem with a “contaminated” reference group. At baseline in our previous study among women (3), there are inverse correlations between reported intakes of different non-fermented milk products; the Swedish market provides mainly three types of milk based on fat content: 0.5% fat, 1.5% fat, and 3% fat milk. Thus, low fat (0.5%) milk intake has a correlation of -0.18 (p<0.00001) with 1.5% fat milk and a correlation of -0.22 with 3% fat milk (p<0.00001). More importantly, 45% of women consuming <1 glass reduced fat milk/day (0.5% or 1.5% fat) consumed 1 glass or more of 3% fat milk/day and 64% of women consuming <1 glass 3% fat milk/day consumed 1 glass or more of reduced fat milk. If the pattern is similar in the US cohorts, the reference categories in Table 3 will consist of not only less than one serving of the subtype of milk but a mixture of low consumption of the exposure and higher consumption of other milk subtypes. We now provide non-fermented milk product specific results based on our previous study (3) illustrating the consequences of a mixed reference category (Table: http://admin.webb.uu.se/infoglueDeliverWorking/digitalAssets/823/c_82363...), also highlighting the different exposure widths used in the US studies and in our Swedish setting.
Specifically, the results are different when consumers of other non-fermented milk types are kept in or excluded from the analysis when subtypes of non-fermented milk consumption (based on fat %) are studied in relation to mortality. When the reference category is “contaminated” with exposure to other milk products, the hazard ratios are clearly attenuated. Adjustments for type of milk influence our estimates only modestly. Moreover, our estimates by use of this approach seems to be compatible with the results from the US cohorts (1) when examining similar exposure categories.
To facilitate the comparison with our previous study (3) and interpretation of their own results, we would like to suggest that the authors run if possible additional analyses in the cohorts using less than one serving/day of total non-fermented milk intake (low and high fat milk in combination) as the reference and 3 servings/day of total non-fermented milk intake or more as the highest category. We assume that few women and men in the cohorts are high consumers of non-fermented milk (more than 3 glasses/servings per day) but we might be wrong.
As mentioned by the authors, a large Japanese cohort study in a population with traditionally low consumption of milk has shown lower mortality rates with “high” consumption of milk (4). Careful evaluation of the exposure reveal that the lowest exposure and reference consisted of never users of milk (zero consumption) while the highest category was consumption of milk almost every day (corresponding to an average of only 100 g/day). This is a considerably different exposure width compared with our Swedish cohorts (3). Of note, non-fermented milk was for long in many families a standard beverage at every meal in Sweden. In total, given the different cohort study results in different populations, there seems to be a U-shaped pattern of mortality with non-fermented milk consumption and we ask the authors (1) to perform the suggested additional analyses to shed further light on this assumption.
An additional concern from our point of view for the interpretation of milk results by use of NHS and HPFS is that no adjustment was made for socioeconomic status, arguably because study participants all initially had a similar high educational level. During 30 years of follow-up considerable changes in family income between study participants may have occurred (5). In contrast to Sweden and Europe (6), milk intake in the US seems to be linked with income and social class (7-11). Can the authors reassure us that our concern is unjustified?
References
1. Ding M, Li J, Qi L, Ellervik C, Zhang X, Manson JE, et al. Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies. BMJ. 2019;367:l6204.
2. Michaelsson K, Wolk A, Melhus H, Byberg L. Milk, Fruit and Vegetable, and Total Antioxidant Intakes in Relation to Mortality Rates: Cohort Studies in Women and Men. Am J Epidemiol. 2017;185(5):345-61.
3. Michaelsson K, Wolk A, Langenskiold S, Basu S, Warensjo Lemming E, Melhus H, et al. Milk intake and risk of mortality and fractures in women and men: cohort studies. BMJ. 2014;349:g6015.
4. Wang C, Yatsuya H, Tamakoshi K, Iso H, Tamakoshi A. Milk drinking and mortality: findings from the Japan collaborative cohort study. J Epidemiol. 2015;25(1):66-73.
5. Lee S, Kawachi I, Berkman LF, Grodstein F. Education, other socioeconomic indicators, and cognitive function. American journal of epidemiology. 2003;157(8):712-20.
6. Darmon N, Drewnowski A. Does social class predict diet quality? The American journal of clinical nutrition. 2008;87(5):1107-17.
7. Kirkpatrick SI, Dodd KW, Reedy J, Krebs-Smith SM. Income and race/ethnicity are associated with adherence to food-based dietary guidance among US adults and children. J Acad Nutr Diet. 2012;112(5):624-35 e6.
8. Ervin RB, Wright JD, Kennedy-Stephenson J. Use of dietary supplements in the United States, 1988-94. Vital Health Stat 11. 1999(244):i-iii, 1-14.
9. Davis CG, Yen ST, Dong D, Blayney DP. Assessing economic and demographic factors that influence United States dairy demand. J Dairy Sci. 2011;94(7):3715-23.
10. Stewart HD, D. Carlson, A. Is Generational Change Contributing to the Decline in Fluid Milk Consumption? Journal of Agricultural and Resource Economics, Western Agricultural Economics Association. 2012;37(3):1-20.
11. Dubois L, Girard M. Social position and nutrition: a gradient relationship in Canada and the USA. Eur J Clin Nutr. 2001;55(5):366-73.
Competing interests: No competing interests
What do the findings mean for people who have a vegan diet?
The article focuses predominantly on the negative impact of high dairy intake. However, if I interpret the findings correctly, this study suggests that a zero dairy intake is associated with higher all-cause and cardiovascular mortality compared to moderate dairy intake. What should I say to patients in my clinic who are vegan?
Competing interests: No competing interests
The study is very detailed and wonderful.
Rather than generalising the term dairy we should think about the utility of each type of milk taken up.
For instance, as per today’s norms, we get milk as a formulated product mixing various kinds of sources right from cow's milk to soya milk. When we look back at complementary medicines likethe ancient Indian system of medicine - Ayurveda - there is systematic interpretation of each source of milk: its qualities and its benefits and ill effects. There are eight different sources of milk explained in the Indian science, as well as those who can use what source of milk and dairy products. From clarified butter to butter and curd the utility, mode of usage, seasons of usage, time of usage and other details can be obtained in the classical ancient scriptures. Interpretations from lactose intolerance to dairy product intolerance is evaluated as technology progresses. This might lead us to a very generalised view about the intake of dairy products. Everything is not good for everyone, so then we need to think about the basic resources: when, where, for whom and how to intelligently utilise the resources available.
Competing interests: No competing interests
Response to Prasanth Dharmarajan, David Newby, Karl Michaëlsson, George Henderson, Jiaoyan Ren, JK Anand, and Tuyen Duong
Response to Prasanth Dharmarajan
Our cohort is located in the US and dairy products are predominantly from cow's milk. We did not include soymilk or butter in our paper. The public health implication for the general population is that high dairy intake (>=3 servings per day) was not associated with lower risk of total mortality.
Response to David Newby
In a dose-response analysis, we showed that moderate dairy intake was associated with slightly lower risk of total and cardiovascular mortality, although the effect size was small. Thus, our conclusion is that high dairy intake was not associated with lower risk of mortality.
In our study, we did not specifically restrict to participants with a vegan diet. However, in our stratified analysis, we stratified by diet quality (high vs. low). The high-quality diet was featured by high intake of fruits, vegetables, and other plant foods. The association between dairy intake and mortality was similar between individuals with low and high dairy intakes.
Response to Karl Michaëlsson
We appreciate Dr. Michaëlsson’s great comments on our paper. We presented intakes of subtypes of dairy products as well as intake of fruits and vegetables according to intakes of total dairy products in Table R1.
In table 3 of our paper, we categorized exposures differently for subtypes of dairy products. This was based on the amount of consumption in the overall population (the average amount of whole milk intake was low, and we used <1/month as reference group), and we categorized them differently to have sufficient number of participants in each category. We understand Dr. Michaëlsson’s concerns about the effect of different cutoff points of exposure on the results, and thus we have presented HR per increment of 0.5 serving/day, which was not affected by cutoff points of exposure and different definition of reference groups.
Dr. Michaëlsson mentioned that the reference categories in Table 3 consisted of not only less than one serving of the subtype of milk but a mixture of low consumption of the exposure and higher consumption of other milk subtypes. We addressed this issue by mutually adjusting for individual dairy products in the analyses. Taking whole milk as an example, the interpretation of our findings was that the HR of mortality comparing other categories of whole milk to the reference category while holding intake of other types of dairy products constant.
We have run additional analysis to examine the associations of non-fermented milk intake with risk of mortality as Dr. Michaëlsson suggested. We used cutoff <1/wk, 1-4/wk, 4/wk-1.5/d, and≥1.5/d to be consistent with our paper and presented the HR and P value for per serving increment in milk intake. We found that higher intake of total milk was associated with slightly higher risk of total and CVD mortality (3-5%).
We did not include socioeconomic status as a covariate, as all participants were nurses or health professionals. We acknowledge that this might affect the generalizability of our results to the overall population, however, the health professional status of the participants allowed us to collect high quality data over a long period of follow-up. Our previous findings on other diet and lifestyle factors and chronic disease risk have been consistent with results from other populations with different SES and racial and ethnic composition.
Table R1. Mean intakes of subtypes of dairy products, fruit, and vegetables according to frequency of total dairy consumption at baseline in the NHS, NHS2, HPFS.
NHS NHS2 HPFS
Characteristics
(servings/d) Q1 Q3 Q5 Q1 Q3 Q5 Q1 Q3 Q5
Skim milk 0.11 0.56 1.56 0.30 0.85 1.55 0.12 0.54 1.91
Cheese 0.31 0.71 1.00 0.26 0.50 0.79 0.23 0.55 0.87
Whole milk 0.05 0.17 0.38 0.03 0.06 0.12 0.03 0.11 0.38
Yogurt 0.03 0.11 0.17 0.05 0.12 0.18 0.03 0.08 0.13
Ice cream 0.09 0.21 0.28 0.06 0.10 0.15 0.08 0.19 0.27
Cream 0.06 0.15 0.75 0.11 0.87 3.94 0.04 0.12 0.57
Sherbert 0.02 0.05 0.07 0.07 0.13 0.17 0.03 0.06 0.09
Vegetables 2.48 2.96 3.14 2.56 2.89 3.19 2.86 3.03 3.15
Fruit 1.11 1.49 1.68 0.98 1.15 1.35 1.43 1.60 1.79
Response to George Henderson
Dr. Henderson’s main concern is about the associations of dairy intake with total energy intake and BMI shown in Table 1: Dairy intake was positively associated with total energy intake, a risk factor of obesity, however, no association appear to be found for BMI. In table 1, all numbers presented were only age-adjusted. Although dairy intake was positively associated with total energy intake, it was also associated with higher amount of physical activity and lower proportion of current smokers. Thus, it is highly likely that dairy intake was not associated with BMI in the presence of a positive association with total energy intake. In fact, the associations of dairy products with a variety of covariates showed the importance of multivariate-adjusted results as presented in Tables 2-4.
Response to Jiaoyan Ren
We thank Dr. Ren for the great questions on the mode of delivery and breast feeding in early life. We have obtained information from the mother’s questionnaire of NHSII participants. In total, we have 32638 participants with 548 mortality cases documented. Only 3% of them were delivered by c-section and 54% of the Nurses were fed by breast milk in early life. We additionally included mode of delivery and breast feeding as covariates, and the results did not materially change. Although we did not obtain the information among older populations in the NHS and HPFS, we believe the c-section rate was even lower among these participants and the effect on the associations between dairy and mortality is minimal.
We agree with Dr. Ren that thermal processing may affect the digestibility and digestion
kinetics of milk proteins and other nutrients. However, dairy products consumed in the US are predominantly commercial products, the processing procedure of which is strictly controlled and standardized. While the processing procedure differs across subtypes of dairy foods including yogurt, milk, and cheese, we did not expect much variation in processing procedure within each subtype of dairy foods.
As to subtypes of yogurt including plain yogurt and yogurt with added sugar, we did not ask the information in the food frequency questionnaire to conduct further analysis.
Response to JK Anand
Thank you for sharing the knowledge on dairy products from different species. Our study is based in the U.S., and as you mentioned, dairy products are almost exclusively from the cow. Thus, our results are unlikely to be affected by mammal species. As dairy products are predominantly from the cow in the Europe, US, and Asian countries, the inconsistency among results found in different cohorts located in the Europe, US, and Asia may be due to differences in background diet, consumption patterns and population characteristics rather than dairy products from different mammal species.
Response to Tuyen Duong
We agree with Duong that dairy products may not be recommended for special groups of the population, such as patients with chronic renal failure. However, our population was sampled from overall population, and the public health implication that “high dairy intake was not associated with lower risk of mortality” is applicable to the general population.
As to the two clinical trials Duong mentioned, dairy products used in the “high-dairy diet” was low-fat dairy products including semi-skimmed yoghurt, reduced-fat cheese, and semi-skimmed milk and/or buttermilk. One study showed that high-dairy diet has no effect on blood glucose,2 and the other study showed that high-dairy intake resulted in a reduction of blood pressure.3 Given the short follow-up time of the trial and modest effect size, the effect of high-dairy intake on long-term outcomes such as mortality are likely to be small, as documented in our studies.4-6
Reference
1. Michaelsson K, Wolk A, Langenskiold S, et al. Milk intake and risk of mortality and fractures in women and men: cohort studies. BMJ 2014;349:g6015.
2. Eelderink C, Rietsema S, van Vliet IMY, et al. The effect of high compared with low dairy consumption on glucose metabolism, insulin sensitivity, and metabolic flexibility in overweight adults: a randomized crossover trial. Am J Clin Nutr 2019;109:1555-68.
3. Rietsema S, Eelderink C, Joustra ML, et al. Effect of high compared with low dairy intake on blood pressure in overweight middle-aged adults: results of a randomized crossover intervention study. Am J Clin Nutr 2019;110:340-8.
4. Ding M, Huang T, Bergholdt HK, et al. Dairy consumption, systolic blood pressure, and risk of hypertension: Mendelian randomization study. BMJ 2017;356:j1000.
5. Ding M, Li J, Qi L, et al. Associations of dairy intake with risk of mortality in women and men: three prospective cohort studies. BMJ 2019;367:l6204.
6. Drouin-Chartier JP, Li Y, Ardisson Korat AV, et al. Changes in dairy product consumption and risk of type 2 diabetes: results from 3 large prospective cohorts of US men and women. Am J Clin Nutr 2019;110:1201-12.
Competing interests: No competing interests