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    Food Additives Food Additives & Contaminants: Part A Contaminants ISSN: (Print) (Online) Journal homepage: htps:/¥w.tandifonline.com/lo\ttac20 Assessment of aflatoxin M, exposure and associated determinants in children from Lahore, Pakistan Waseela Ashraf, Abdul Rehman, Mansur-ud-Din Ahmad, Masood Rabbani, Muhammad Hassan Mushtaq, Khalida Aamir, Fareeha Akhtar & Jia-Sheng Wang To cite this article: Waseela Ashraf, Abdul Rehman, Mansur-ud-Din Ahmad, Masood Rabbani, Muhammad Hassan Mushtaq, Khalida Aamir, Fareeha Akhtar & Jia-Sheng Wang (2022): ‘Assessment of aflatoxin M, exposure and associated determinants in children from Lahore, Pakistan, Food Additives & Contaminants: Part A, DOI: 10.1080/19440049,2022.2138559 To link to this articl 2 https://doi.org/10.1080/19440049,2022,2138559 A) runic onine27 oe 202 CF suvmityourartice to this journal CA EER view rotated artcies ® View crossmark data? Full Terms & Conditions of access and use can be found at heepsiswaw.tandfonline.cam/action/jaurnalinformation2journalCode=tfac20 Freie 018m" 34909 20222150559 Taylor & Francis, cst nin Assessment of aflatoxin M, exposure and associated determinants in children from Lahore, Pakistan Waseela Ashraf” @, Abdul Rehman* @, Mansur-ud-Din Ahmad”, Masood Rabbani“ ©, Muhammad Hassan Mushtaq*, Khalida Aamir’, Fareeha Akhtar® and Jia-Sheng Wang” @ Department of Epidemiology and Public Heath, University of Veterinary and Animal Sciences, Lahore, Pakistan; “Department of Environmental Health Science, The Univesity of Georgia, Athens, GA, USA ‘Istitue of Microbiology, Unversy of Veterinary and ‘Animal Seience, Lahore, Pakistan; “Department of Preventive Pediatric Medicine, The Children’s Hospital and The Institute of Child Health Lahore, Pakistan ‘Aflatoxin are potent carcinogenic and immunomodulatory mycotoxins, and exposure may lead to deleterious effects on human health. This study aimed to detect aflatoxin M, (AFM) 2s biomarker of exposure and determine associated risk factors in children attending a spe- Calized:1000 mL. Most of the children, ie. 67.2% (160/238) had eaten dry fruits; 60.9% (145/238) eggs; 60.1% (143/238) yogurt; 40.3% (96/238) meat; 9.2% (22/238) cold storage food, while 7.6% (18/238) had consumed butter in the last 72h before sample collection. Amongst 28.2% (67/238) children (< 2years old), a small propor- tion was breastfeeding ~ 37.3% (25/67), while the rest of them completely relied on milk from other sources. Weaning age of most children (99.1%) was 6months or earlier, while for the remaining children (0.9%) it was not known (Table 2), Prevalence of AFM, and associated risk factors ‘The overall prevalence of urinary AFM, was 65.5% (156/238). Frequency distributions of urin ary AFM, positivity along with other factors, eg. demographic, and socio-economic factors, daily dietary intake, and participant's general health information, are presented in Table 2. Results of multivariable analysis showed that the prevalence was significantly higher (p= 0.001) in hot-humid season (74.6%, 85/114) compared to cold-dry sea- son (57.3%, 71/124). The participants from hot- humid season had double odds (OR = 2.64, 95% Cl = 149-479) of having urinary AFM, com- pared to participants in cold-dry season. Similarly, residence area (rural vs urban) was also significantly associated (p=0.007) with the occurrence of AFM,, and participants who used to live in urban settings had about 2.21 (95% Cl = 1.25-3.97) times higher chances of AFM, exposure as compared to participants from rural settings (Table 3), Results of univariable analysis indicated that urinary AFM, prevalence was higher in children; who's guardians were not aware of the possible milk contamination (p=0.035), and who used cold storage food during the last 72h (p =0.034). However, these attributes were insignificant in the multivariable analysis. Further, the source of dairy products, mothers’ knowledge about milk 000 ADOVTVES& CONTAMINANTS: PART A) 5 safety, and consumption of animal products (ic. milk, meat, and butter) were not significantly associated with the occurrence of urinary AFM). ‘The median urinary level of non-creatinine- adjusted AFM, was 0.57 ng/mL (QI-Q3= 0.23-14 ng/mL), while the median urinary level of creatinine-adjusted AFM, was L.9ng/mg cre- atinine (Q1-Q3 ~0.82-6.0ng/mg creatinine). The children in age group <2 presented significantly higher (p=0.037) urinary AFM, (median 3.2ng/mg creatinine) compared to children in age group >2 years (1.6ng/mg creatinine) (Table 4), Similarly, children undergoing nutrition clinic (32ng/mg. creatinine) had noticeably higher AFM, levels (p=0.003) compared to those of general OPD subjects (14ng/mg creatinine). Furthermore, mother’s perception about child nourishment (malnourished = 2.6 ng/mg creatin- ine versus well-nourished = 14ng/mg creatinine, p=0.042) and quantity of milk consumed by child (250-499=1.6ng/mg creatinine versus 500-1000=2.4ng/mg creatinine —_versus >1000=5.6ng/mg creatinine, p=0.048) were also statistically significant (Figure 1). Discussion ‘The monitoring of human urinary AFM, is essential in order to establish a baseline for APs exposure through the food chain, We found that two-thirds of the children (65.5%, 156/238) were positive for AFM,. These results are in agreement with a recent and first investigation on urinary APM, in children and adults from Pakistan which reported similar prevalence (69%, 182/264) (Xia et al. 2020). ‘The sustained exposure of AFs might be due to the lack of standardized uniform legislation for different food commodities and poor testing facilities present in Pakistan. However, another study from urban settings in Punjab province found that only 11.3% (17/150) of children were positive for AFM, (Nasir et al 2021). Furthermore, in the current study, the urinary level of AFM, was higher (creatinine- adjusted = 1.9ng/mg creatinine, while non-cre- atinine-adjusted = 0.57ng/mL) than previous studies from Pakistan (range = 0.125-2.529 ng/ mL by Nasir et al 2021; mean = 0.023 + 0.048 ng/mL. by Xia et al, 2020). A higher 6 @ WASH Er AL Table 2. Summary of variables included in univariable analysis to determine the association with aflatoxin My positivity in chi dren in Lahore (n= 238) Tested Pose arabes categories 100) nts pale Demographic and sodeeconomic factor Age bea) 2 67 282) 4510.2) 0768 32 mana m1 643) ender Female a 2a) 641634) ose ae 137673) 921602) Eduction lvl of mathe Format 160672) 108 (673) 0386 Inoral 78 628) 481615) Employment of father/quarian Soverment 521) 5 (10) ott Prete 24.621) 7762) Saemployed 107 (43) 731682) Unemployed 2008) 1300) Income lvelimonth (US Dols) 1a 138 573) 92667) 81 Swe 10 2) 62 (6t0) Residence locaton ban 135 (8:2) 5671) 010 fu 103 1432) (583) umber of sings ey 167 (702) 101659) ome Sa 71 098) 46 648) Sexson Hoehumié Summer 114479) 046) 06" Winter 24.620) 71573) Factors elated 10 consumption of mk and mik products Source of mk forthe omy enaladaiy 10420) 70,700) oss racy shop 191798) 11673) Household 62 268) fia) ik shop 5 238) 35 (625) ak purchase preferences Fresh ik 219 920) 5 (662) 1.00 Processed mk 90738) 11 878) Sourcetype of mk purchase Butao 17 45) wien oss cow 52.018) 3722) es a9) 34723) adage 1975) 11579) Do nat know 1346) i615) uzatlon fr using the same mie source (months) ou 137 (785) 15 55) ar en 34 (143) 23108) Change often van 1a 88) ik cuantity purchased a) 35 2038) 1450) ost 052 176735) 1141648) 255 52 218) 35 (673) Dy ik 8036) 41500) a says safe ve 208 653) 138 669) ono No 313) 21667) Do not know 2a) 16.551) ha can be contaminated ves 12600) 4033) oss? No 200 40) 137 (683) Do not know 25 (103) 15.575) Source for day products Homemode. 51.014) 30 (583) sae Market 17 (45) 1194672) Both ota) 7 0) "Ty of mk consumed by the cid Mater eed 25.105) 16 (64) ons Otter ures! 215 695) 140 (657) ‘Quantity of mk consumed per day (mk) bythe eid 230-408, 161 (76) 102 (634) 0660 50-1000 70 094) 49.00), “000 729) 014) Yogurt consumption by the child Yer 143 (601) 9657) 1.00 No 95 693) 21653) suter Yes i} 10559) os No 2201824) 146 63) Consumption of ether fod ams by the cid during ast 72 too ves 145 (605) 58 648) om No 93 691) ater Meat ves 96 403) 50613) 03st No 142 692) 57 683) old storage food Yes 2292) 19 68) ose" No 216,908) 137164) Dy fruits Yes 160672) 102 (6.8) 0468 No 78 6528) 581692) Child heated information Partpant visting Several 0°O 149 (63) 103 (602) sor Nutton da 2907 53593) (continued) Table 2. Continued F000 ADOVTVES & CONTAMINANTS: PART A) 7 Teed ove orale Caegories 209) a0) pale ‘ge at which complementary diet stared “6 months 6 67 91563) a6 26 montis 220 624) 145 (659) De not know 2109) 2100) ft vaccination (nine) Complete 218,902) 15 (671) ose Incomplete 202) 11650) Phys aches Moe patcpatve 228 (958) 150657) or Less paricpatwe 142 (60) Mosher satisction about child growth Ye 94 595) om ost No 125 625) 77616) Do not know ‘91798) 101525) Mer perception about cid nourishment Malnourished 98 12) 83 697) ox Wel ourhed 0 (588) 8 483) Frequency of ness Frequently 15 569) 56 (636) ors Not frequen 150 1630) 100 15.7 owuffloomaa mik Expanded program on immunization. variable hot had ple 0.2 were selected or mulvorble analy Table 3. Summary of variables retained in the final multva able logistic regression model (n ~ 238 arable Response categony 0465 to CL RS-97S¥) pale Season Winter Reference ‘0001 Hothumid summer 24 149-479 Resident ural Reference 007 ion 221 125-397 te ‘ise prevalence and urinary AFM, levels in the cur- rent study could be due to the difference in the geographical location, as due to high humidity Lahore (the current study area) is more favour- able region for fungal growth compared to Multan, Similarly, in contrast to Nasir et al. (2021), we also collected samples during humid summer season (je, August and September) in addition to winter (February) and dry-summer months (March-July) that might have increased the prevalence and urinary AFM, levels in our samples. Another factor could be related to the selection of the sampled group as the earlier work was carried out on apparently healthy chil- dren compared to our participants who were pre- sented to the hospital for various health issues. ‘Also, in the previous studies, about one-third participants were not consuming milk which is one of the major food items contaminated with AFM,, In Lahore, there are number of peri-urban farms to fulfil the milk demand of this big popu- lation and the mean values of AFM, in milk in different studies from Lahore ranged from 0.232 to 17.38 g/L which is high, and this might have resulted in a relatively higher urinary AFM, levels in children (Yunus et al. 2020: mean = 4.84 pg/L, Ahmad et al. 2019: mean = 0.23 pg/L, Aslam et al. 2016: mean = 2.58, Muhammad et al. 2010: mean = 17.38ug/L.). Over and above, we also evaluated our participants for AFBy-lyse adduct levels in serum through High-performance liquid chromatography (HPLC) and all participants were positive with median levels 10.66 pg/mg albumin (Q1-Q3=6.25-20.32) which indicates a higher exposure to aflatoxins (Ashraf et al. 2022). ‘Nevertheless, the prevalence of APM, in other countries also varies. Researchers from Malaysia reported a wide range of prevalence of urinary APM, in children (40.8-100%) (Redzwan et al. 2012; Sabran et al. 2012a, 2012b; Ahmad et al. 2020). Similarly, studies from Nigeria and Iran reported 99% (83/84) and 21% (15/70) prevalence (Mason et al. 2015; Ezekiel et al. 2018). A recent Ethiopian study in school children (6-12 years of age) found that urinary AFM, levels were 0.48ng/mg creatinine (QI-Q3: 0.203-1.085 ng/ mg creatinine) (Gebreegziabher et al. 2022), Similarly, a study from Ghana found urinary AFM, levels of mean 1.8ng/mg creatinine (Jolly ct al, 2006). Another study from Ghana detected a higher level of urinary AFM), ie. 2.16ng/mg creatinine (Kumi et al. 2015). The variation in prevalence and urinary AFM, levels could be attributed to several factors, including socioeco- nomic differences in the study population, sample size variation, genetic susceptibility to aflatoxins, type of test used, aflatoxin exposure levels, health and nutritional status of the individuals, food safety standards implemented in the region, hygiene practices followed, and climate of the 8 @ WASH Er AL ‘Table 4. Associaton of various factors with aflatoxin M, concentrations in urine samples of participants—only positive individuals. were included in the analysis (a = 156). sive Median AFM, Medan AF arabes Caregosies * inginl) aging cestnine) __ pValue Demographic and socoeconomic ator Age bea) 2 6 0 a2 oon 32 ™m 056 16 ender Female 6 035 13 0964 ae 2 038 18 Eduction lvl of mathe Ferma 18 036 18 0965 Informal 4% 060 19 Employment of father overment % 025 os owe? rte n 068 29 Sa employed B ost 16 Unemployed a 095 8 Income levelmonth (US dots) 1a 2 sr 29 oz Se a 280 iS Location Ubon 36 056 8 0581 ful a 068 19 umber of sings ey ro oss 18 ons oa 4 068 19 Sean Hothumd summer 8S 070 7 om Winer n 088 ae Factors elated to consumption of mk and mik products Source of mk Sevaa/aiy 70 068 1 ons Grocery shop " 07 26 Household, “0 oar i lk shop 5 030 19 ak purchase preferences Fresh us 036 18 ry Proceed " on 26 Sourcetype of mk purchased for family consumption Blo 6 ost 15 0851 Cow a 075 18 Mees se ose 8 Paclages 0 07 26 Do nat know a oar a uzaton for using the same mie source (months) uy a 035 u ost eu 2 oat 26 Change often 0 oa 1 ik cuantity purchased a) 35 o 14 26 0961 052 ne vy 18 2555 5 052 a Dy ik o oz 13 a says safe ve 138 060 a ow? No a Fr ” Do not know 16 as 25 at canbe contaminated Yee o 19 a8 030 No 7 099 ir Do not know 5 as 2s Source for day products Home made x0 oa 3 ose Shop 19 068 13 Bath o 0 14 "Tye of mk consumed by the cid Mater eed 16 oa 20 ons Other sures! wo 080 13 ‘Quantity of milk consumed per day (ml) bythe child 250-499 1a oa 18 ote" S0-t000 2 oar a 000 & 15 Sa Yogurt consumption by the child Yes 3 036 056 on No e 09 030 suter Yes 10 033 14 owe No 6. 060 13 Consumption of ether food ams too ves * oss Ww 0309 No a 066 2 Mest Yes 9 oa 14 om No 7 060 aa old storage food Yes 9 043 096 on No 7 039 13 Dy fruits Yes a2 058 7 os No se 038 a7 Child heated information Partpant visting Sener PO 1s 086 “ 0003" Nutton cn 2 0 2 (continued) Table 4. Continued 000 ADOVTVES& CONTAMINANTS: PART A) 9 Feitie— Wedan nh———dan oral cages 7 Tog) aging. ete) _—_pYae foe ih compen Gi a Emons % 06s ‘a ona Seino ica oe % Baro know o “ % {9 acon Ge) Comte ts Os ta oso Farce in seats tre i te 3 586 tee oe tas 2 Mote sso about cdrom te o tae % os9 te ” on B Be ot know w ar a others ection abou il crshnent toured % ae ie oon Metrouhed tan wa Fremanc of ess Freie % oe ag oma Novregvnty ao a ie Fewboons wi ‘td pgm on mtn Yer andjed tough Wc ok som and Ks Wis tes 156 A B & § 2 2 ir a 2 T = 7 2 » tosi-2000 250-540-1080 Cottage san) Daly Mi Consumption) c D ge i = fs fo Bo Ev a zy g = r + Nation tne op (Cild Visiting Ctild Matpourished Figure 1. Comparison of the mecian urinary AFM between participants based on (A) child age in years (p = 0.037). (B) Daily mile consumption in mL by child about child nourishment (p = 0.042). Logcransformed values for uri study area. However, the crucial determinant for urinary AFM, is aflatoxin intake through diet (lly et al. 2006) We also investigated demographic and socioe- conomic factors and dietary habits of the partici- pants that could be associated with the occurrence of urinary APM, as identified by other researchers (Dosman et al. 2001; Sabran 0.088) (C) Child attending/isiing the hospital department (p= 0.003). (D) Mother's perception mary AFM, were used et al. 2012). The study revealed that the exposure risk of AFM, was significantly higher in hot- humid season (p =0.001), and the odds of having APM, exposure were about two times higher as compared to winter season (OR = 2.64, 95% CI 1.49-4.79). This finding agrees with the inves- tigation conducted in Sierra Leone in children (Jonsyn-Ellis 2001) and a study from Pakistan 10 © W.ASHRAF ETAL where authors reported higher concentrations of AFM, in consumer milk during hot-humid se. son (2.59yig/L) (Aslam et al. 2016). Climatic fac- tors, especially environmental temperature, and humidity, strongly affect fungal growth and, hence, AFs production. The climate in most parts of the country is tropical or subtropical, which increases the risk of APS contamination in vari- ous feed and food items and therefore more efforts are required to control this problem. AFM: prevalence was significantly higher (71.1%, 96/135) in urban population than in rural communities (58.3%, 58/103), and the odds of AFM, positivity in children from the urban area were 2.21 times higher (95% CI = 1.25-3.97; p=0.007) compared to participants from the rural areas. This might be due to the differences in urban and rural setups as the burden of the population poses more food demand, leading to more food storage in urban settings. In addition, environmental factors such as humidity and high temperature due to urbanization, promote favourable conditions for fungal__growth. Moreover, from Lahore, 81% (68/84) milk sam- ples exceeded the US FDA and EU limits, raising questions about the storage conditions for feed ingredients (Muhammad et al. 2010). These results are concurrent with reports from Xia et al. (2020), Ezekiel et al. (2018), Ediage et al. (2013), and Ali et al. (2017). ‘The children in age group < 2years were found to exhibit higher AFM, levels. (3.2.ng/mg creatinine) as compared to children in age group >2years (1.6ng/mg creatinine) and this differ- ence was statistically significant (p=0.037). This finding might be due to the low proportion of breastfeeding children (37.3%). Also, due to tran- sition from liquid to solid food in this age group, intake of milk from other sources is usually greater compared to children with age >2 years. These results are in agreement with a previous study from Cameroon where partially breastfed children had higher urinary AFM, levels (1.43 ng/ mL) than fully weaned children (0.28 ng/ml.) (Ediage et al. 2013), Also, in Pakistani culture, introduction to solid food usually contains milk- based food-items (eg. yogurt, Kheer, Pudding, Custard, etc.). This can lead to a high estimation of daily intake (EDI) of AFM; in this age group. A study from Guangzhou, China reported a higher EDI in the lower age group (Zhang et al, 2020). Moreover, many researchers examined dietary patterns when evaluating AFM, exposure in the population of interest. Milk and milk products are among the core components of children’s diet and are more prone to AFM; contamination; hence we determined their association with urin- ary AFM; levels in children. Also, with increased milk consumption urinary AFM, levels also increased (250-499= 1.6 ng/mg creatinine versus 500-1000=24ng/mg creatinine versus >1000=5.6ng/mg creatinine). Similar findings have been reported by Mahdavi et al. from Iran, where AFM, levels were significantly associated (p <0.001) with milk consumption and cow milk was the main source of AFM, contamination (Mahdavi et al. 2010). Nevertheless, in other studies, age has been found to have a positive association with AFs levels (Sun et al. 1999; Almad et al. 2020). This might be due to differ- ences in food intake habits and propensity of individuals of different ages to metabolize and excrete AFs from their bodies after metabolic processing. Also, in our study the age range was 1-11 years, whereas others have included partici- pants from a wide range, ie, up to 80years (Sun et al, 1999; Sulaiman et al, 2018; Ahmad et al 2020; Xia et al. 2020). Some other demographic factors like employment status, family income, and education were not significantly associated with AFM, which agrees with reports from household surveys in the United States (Baker 2003) and Malaysia (Ahmad et al. 2020), As we targeted the population from a hospital and wanted more information on aflatoxin expos- ure, children who were attending the nutrition clinic of the hospital had noticeably higher urin- ary AFM, levels (3.2 ng/mg creatinine, p = 0.003) compared to children who presented to general OPD (1.4 ng/mg creatinine). Furthermore, moth- ers’ perception about child nourishment status was also significantly associated with urinary APM; levels (malnourished = 2.6ng/mg creatin- ine vs well-nourished = 14ng/mg creatinine, p=0.042) (Figure 1). These findings suggest that higher APM, con- tamination in’ milk might be _ significantly contributing to poor child growth in the country. ‘The National Nutritional Surveys from Pakistan evidently reported higher prevalence of malnutri- tion in children from 2001 to 2018 (UNICEF Pakistan 2019). People who used packaged milk tended to have higher AFM, exposure (median 2.6ng/mg creatinine) than those who consumed fresh milk (median = 1.8ng/mg creatinine). Moreover, most of the parents/guardians (86.9%) stated that milk was always safe and free of con- taminants, which highlights the need for an edu- cation program for the public. Our study provides data on AFM, exposure in children coming to a tertiary care hospital in the Lahore district. More than half of the children were posi- tive for urinary AFM,, and the exposure in chil- dren was higher in the urban area and during hot-humid season. Children who consumed higher quantities of milk, attended nut clinic and whose mothers were not satisfied from nutrition had higher urinary AFM, levels However, longitudinal studies are required to investigate and assess the impact of AFs exposure in Pakistani children, Therefore, there is a dire need to establish a uniform mitigation strategy focusing on improving food quality through strict control measures and public awareness programs throughout the country. In addition, mothers should be encouraged to breastfeed their young ones instead of providing animal/formula milk to reduce exposure to AFM, Acknowledgements ‘The authors are thankful to the children and their parents! guardians for their cooperation during the study. The authors thank the Higher Education Commission, Islamabad, Pakistan for providing Ph.D. fellowship to Ms ‘Waseela Ashraf under the indigenous scholarship program [Ref No. 315-3071-2883-061(50034121)], This research paper isa part of her PAD work, Disclosure statement No potential conflict of interest was the author(s) reported by Funding ‘This research was funded by the Higher Education Commission (HEC), Pakistan, FOOD ADDITIVES & CONTAMINANTS: PART A.) 11 ‘oRcID Weseel Ashraf ® http:/Forcd.org/1000. 0002-2236 8581 Abdul Rehman © hitpl/orid.og/0000-000-6290.2999 Masood Rabbani @ hitpl/orcid.ong/0000-0001-6777-1879 Jia Sheng Wang @ hip/orckd.org/9000-0002- 8458-9187 References Ahmad F, Jamaluddin R, Esa NM. 2020. 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