Association between milk consumption and lactose malabsorption in Indonesian children

Syarimonitha Munadzilah,Badriul Hegar,Rini Sekartini,Yvan Vandenplas

(1.Department of Child Health,Faculty of Medicine Universitas Indonesia,Dr.Cipto Mangunkusumo Hospital,Jakarta,Indonesia;2.Kidz Health Castle,UZ Brussel,Vrije Universiteit Brussel,Brussels,Belgium)

Abstract:Objective To study the association between milk consumption and lactose malabsorption in Indonesian children aged 3-12 years.Methods This cross sectional study was conducted in randomly selected presumed healthy children with good nutritional status aged 3-12 years in Central Jakarta,Indonesia(n=174),including 72 children aged 3-5 years and 102 children aged 6-12 years.Results The prevalence of lactose malabsorption in children aged 3-5 years and children aged 6-12 years was 20.8%(15/72)and 35.3%(36/102),respectively.There was no association between milk or milk product consumption and lactose malabsorption(P>0.05).In the 51 children with lactose malabsorption,the predominant clinical symptoms were diarrhea(62%),abdominal pain(52%),and nausea(5%)during the hydrogen breath test.Conclusions There is no association between milk consumption and lactose malabsorption in Indonesian children aged 3-12 years,suggesting that genetic predisposition may be more important than adaptive mechanisms to lactose consumption.

Key words:Lactose malabsorption;Hydrogen breath test;Milk consumption;Prevalence;Child

Lactose malabsorption is a physiological condi‐tion caused by a reduced expression or activity of the enzyme lactase,causing an imbalance between lac‐tose consumption and the amount of active enzyme available[1].Differences in phenotype expression of lactase activity may explain the difference in the prevalence of lactose malabsorption.However,a pro‐longed exposure to lactose(milk and milk products)has also been proposed to induce an adaptive re‐sponse to lactose[1-4].Achange in the dietary consump‐tion of milk and milk products in the Indonesian popu‐lation was observed during the last few decades.According to the national socio-economic survey con‐ducted from 1993 to 2016,there was an increase of milk consumption from 1.86 L per person per year to an average consumption of 11-12 L per person per year[5].The current study was conducted to determine the current prevalence of lactose malabsorption in In‐donesian children aged 3-12 years.These findings were compared with the historical data[6-8].This study evaluated the association between milk consumption and lactose malabsorption.We also determined the clinical symptoms that occurred after exposure to milk and milk products in children with lactose malab‐sorption.

1 Material and methods

1.1 Subjects

This cross sectional study was conducted in ran‐domly selected presumed healthy children with good nutritional status aged 3-12 years in Central Jakarta,Indonesia.The nutritional status was determined for each subject based on weight/height WHO child growth standard (https://www.who.int/tools/childgrowth-standards/standards).

Exclusion criteria were children who were not presumed healthy or had a history of probiotic or anti‐biotic intake during the two weeks preceding the hy‐drogen breath test[1].Parents were informed not to allow their children to consume bread,potatoes,corn or fiber the evening and night before the breath test and were excluded if they did.Parents gave their informed consent to participate.

1.2 Data collection

The information regarding the consumption of milk and milk products by the children and parents was recorded by using a retrospective questionnaire regarding dietary habits.The categories of milk and dairy products and their lactose content consumed were estimated according to the Food and Drug Ad‐ministration recommendations for each food serving size[9].A glass of milk is about 200 mL,which con‐tains 12 g of lactose.Ice cream accounts for 1/2 cup,thus containing 6 g of lactose,a portion of yoghurt contains 8 g of lactose,and one portion of cheese ac‐counts for 30 g containing less than 0.5 g of lactose.

1.3 Definition of lactose malabsorption

"Lactose malabsorption"is reserved for the chil‐dren in whom the intestinal malabsorption of lactose has been investigated using an appropriate test.A hy‐drogen breath test using the Gastro+TMGastrolyzer?was performed in each participant.The exhaled hydro‐gen was measured after administration of a standard dose of lactose(dosage of lactose:2 g/kg body weight with maximal dosage of 50 g).After a 5 hours fasting period,breath samples were collected through a Steri‐BreathTMmouthpiece.Baseline hydrogen had to be be‐low 20 parts per million(ppm).Half an hour after the lactose intake,the first breath sample was collected,and a new sample taken every 30 minutes during two hours.Lactose malabsorption was defined as an in‐crease in hydrogen concentration with≥20 ppm from baseline[10].Parents and children were asked to record all complaints that occurred after the ingestion of the lactose during to the following 24 hours."Lactose in‐tolerance"is used when gastrointestinal symptoms are experienced after ingestion of lactose.

1.4 Statistical analysis

The study results were statistically analyzed using SPSS software version 22.0,using chi-square or Fisher test with a statistical significance level ofP<0.05.The study protocol was approved by the Medical Research Ethics Committee from the Dr.Cipto Mangunkusumo Hospital in Jakarta,Indonesia.

2 Results

2.1 Characteristics of subjects

A total of 174 subjects were recruited,consisting of 72 children aged 3-5 years and 102 children aged 6-12 years.The characteristics of the participants are shown in Table 1.According to the information ob‐tained by medical history,very few children in both age groups(one child in the 3-5 years group and 3 children in the 6-12 years group)were reported to present gastrointestinal symptoms after consumption of milk and dairy products.It was not known if parents were lactose tolerant or not.

Table 1 Characteristics of subjects

Up to 3 glasses of milk per day was consumed by 80.5%(58/72)children aged 3-5 years but only by 2.9%(3/102)children aged 6-12 years.Most children aged 3-5 years(87.5%)and children aged 6-12 years(81.4%)consumed over 30 g of cheese every day.Yo‐gurt was uncommonly consumed as 98.6% of chil‐dren aged 3-5 years and 76.5% of children aged 6-12 years consumed less than 1 cup per day or do not con‐sume yogurt at all.Twenty-five percentage of children aged 3-5 years consumed ice cream≥1/2 cup every day,while this increased to 84.3% in children in the 6-12-year-old age group.

2.2 Prevalence and symptoms of lactose malab‐sorption

The prevalence of lactose malabsorption based on the results of the hydrogen breath test was 20.8%(15/72)in children aged 3-5 years and 35.3%(36/102)in children aged 6-12 years.

Of the 51 children with lactose malabsorption,21(41%)showed clinical symptoms during the hydro‐gen breath test,including diarrhea in 13 children(62%),abdominal pain in 11 children(52%)and nau‐sea in 1 child(5%)(Table 2).The symptoms appeared after 1-2 hours after the ingestion of lactose and disap‐peared after 5-6 hours.

Table 2 Gastrointestinal symptoms in children with lactose malabsorption (number of cases)

There was no significant difference in the preva‐lence of lactose malabsorption in children aged 3-5 years who consumed 2-3 glasses of milk/day com‐pared to less than 1 glass/day(P=0.51);likewise,in children aged 6-12 years(P=0.70).There was no asso‐ciation between cheese consumption and lactose mal‐absorption in children aged 3-5 years(P=1.00).In children aged 6-12 years,lactose malabsorption did not differ according to the amount of cheese per day consumed(P=0.49).See Table 3.

There was no significant difference in the preva‐lence of lactose malabsorption in children aged 6-12 years who consumed yogurt≥1 cup/day compared to<1 cup/day(P=0.23);likewise,in children aged 3-5 years.The children aged 3-5 years who consumed ice cream≥1/2 cup per day were 2.5 times more likely to experience lactose malabsorption than those in the group who consumed ice cream<1/2 cup/day,but not statistically different(P=0.18).There was no signifi‐cant difference in the prevalence of lactose malabsorp‐tion in children aged 6-12 years who consumed ice cream≥1/2 cup/day compared to<1/2 cup/day(P=0.44).See Table 3.

Table 3 Association between milk and milk products consumption and lactose malabsorption [n(%)]

3 Discussion

The prevalence of lactose malabsorption in chil‐dren aged 3-5 years and children aged 6-12 years was 20.8% and 35.3%,respectively.The prevalence of lac‐tose malabsorption in Indonesian children decreased over time,and was reported to be 71% in 1-6 years old children in 1971,21.3% in 3-5 years old in 1971 and 58% in 6-12 years old in 2001[6-8].A relatively large reduction in the prevalence of lactose malabsorp‐tion was seen in children aged 6-12 years;57.8% in 2017 and 35.3% in the current study.The prevalence of lactose malabsorption in children aged 3-5 years in our study(20.8%)was higher than the prevalence re‐ported in China(12.2%)[11],but lower than the preva‐lence in Malaysia(31%)[12].The prevalence of lactose malabsorption in children aged 6-12 years in our study(35.3%)was similar to the Chinese data for 7-8 years old(33.0%)and for 11-13 years old(31.0%)children[11].The prevalence in Malaysia was reported to be as high as 83%-91%[12].

The term lactose intolerance may not be well un‐derstood by the Indonesian community.Accurate data about the prevalence of lactose intolerance in family members is therefore challenging.The prevalence of genetic lactose intolerance in adults in non-Caucasian countries such as Indonesia is high.The three most common polymorphisms associated with lactase activ‐ity are:homozygous lactase persistent(-13910TT),homozygous lactase non-persistent(-13910CC),and heterozygotes(-13910CT)[13].The genetic polymor‐phism of-13910C>T might influence the difference in lactase activity[9,13].The incidence of non-persis‐tence of lactase activity during infancy in some Asian and African countries is as high as 80%-100%,while lactase persistence in the Caucasian population is 96%-100%[10].In non-Caucasian children,lactase ac‐tivity then gradually declines to low levels in adoles‐cence and adulthood[14-15].Aside from genetic factors,lactase activity has been reported to be affected by continuous lactose exposure over long periods of time[13].Someone who is genetically supposed to have low lactase activity may not experience lactose malabsorp‐tion if the lifestyle of the family includes regular con‐sumption of milk from infancy to adulthood during several generations[6].The Indonesian data provided by Suharjono et al[6](1971)were collected from the general population,whereas Hegar et al[7-8]collected data from the middle and upper socioeconomic popu‐lation.Differences in exposure to milk and various dairy products in 1971,1997 and now,may affect the incidence of lactose malabsorption.The availability and ability to purchase milk might have been quite low in 1971 compared to 26 or 48 years later,which is in line with the increasing economic growth in In‐donesia.In Indonesia,milk and milk product con‐sumption(11.8 L per person per year)has been in‐creasing over the years although this is still lower compared to other countries such as Malaysia(36.2 L per person per year),Myanmar(26.7 L per person per year),Thailand(22.2 L per person per year),and The Philippines(17.8 L per person per year)[5].Our study showed that daily consumption of milk and dairy products has become a routine dietary habit in many children up to the age of 12 years.The vast majority(69/72;95.8%)of children aged 3-5 years were reported to consume at least 2-3 glasses of milk(24-36 g of lactose)per day and 54(52.9%)children aged 6-12 years consume<1 glass of milk(<12 g of lactose)per day.Some dairy products with less lactose content than milk,such as cheese,yogurt and ice cream are al‐so consumed every day by most children in both age groups.In general,the amount of milk and dairy prod‐ucts consumed every day did not show a significant difference in the prevalence of lactose malabsorption.Data obtained in 2003 reported that lactose malab‐sorption in Indonesian children aged 12-15 years who regularly consumed milk was 81.2%,while in chil‐dren who did not regularly consume milk was 69.6%[14].

The development of symptoms after lactose in‐gestion may be influenced by several factors such as the dose,lactase expression,gastric emptying,intesti‐nal motility,microbiome,and production of metabo‐lites by bacteria in colon[1,16].The hydrogen breath test showed lactose malabsorption in 51 children(29.3%)out of 174 children aged 3-12 years;21(41%)of them showed symptoms of lactose intolerance.Data reported by Budiarso et al[14]and Baadkar et al[17],are comparable lactase induction may play a role in those findings[18].In asymptomatic subjects,residual lactase enzyme activity could be higher than in symptomatic subjects.This condition will result in a different amount of lactose that reaches colon.Unfortunately,in this study we were not able to evaluate the level of lac‐tase activity.Clinical symptoms of lactose intolerance vary from person to person.Twelve grams of lactose has been known to be the average amount of lactose tolerated in individuals with genetic lactose malab‐sorption causing symptoms of intolerance[19].

Furthermore,the repeated exposure of the colon to undigested lactose causes fermentation of the lac‐tose resulting in the emergence of a bifidogenic micro‐biota[9].The gastro-intestinal microbiota can adapt to the repeated exposure to lactose.This condition may result in children with lactose malabsorption having a positive hydrogen breath test but remaining asymp‐tomatic[17].Milk consumption may rather indicate that children with milder lactose malabsorption can con‐sume more milk.

Dietary fiber can decrease nutrient absorption and increase gastrointestinal transit time without af‐fecting apparent glucose absorption[1].Fasting breath hydrogen concentrations were significantly lower af‐ter a low-fiber diet[1].Changes in colonic motility dur‐ing active diarrhea could change the partition of co‐lonic hydrogen excretion between breath and flatus with proportionally greater amount of intestinal hydro‐gen being excreted by rectum[20].Therefore,despite suffering intolerance,a hydrogen breath test can give false negative results[21].Rotavirus andGiardia lam‐bliainfections commonly cause(secondary)lactose malabsorption.One study involving 188 infants had a more frequent prevalence of lactose malabsorption in those infected with rotavirus than non-rotavirus diar‐rhea(60% vs 49%,P=0.002)[22].In the current study,we did not evaluate stool specimens for infection be‐cause"presumably healthy children"was the inclu‐sion criterion.Personal hygiene and the environment are also important factors that contribute to intestinal parasitic infections.Unfortunately,we do not have subject and environmental hygiene data.We also did not find any studies comparing the status of lactose malabsorption before and after treatment of parasitic/rotavirus infections.

In conclusions,we observed a decrease in the prevalence of lactose malabsorption in Indonesian children aged 3-12 years compared to the data from 50 years ago.Lactose malabsorption was more fre‐quent in the 6-12 years old group than in the 3-5 years.No association was found between milk and milk product consumption in children aged 3-5 years and 6-12 years with lactose malabsorption.Since no association was found between milk consumption and lactose malabsorption,genetic predisposition may be more important than adaptive mechanisms to con‐sumption of lactose.

Conflict of interest:None of the authors report a potential conflict of interest related to this paper.