Food Chemistry: M. Sager, C.R. Mcculloch, D. Schoder

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Food Chemistry 255 (2018) 365–371

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Heavy metal content and element analysis of infant formula and milk T
powder samples purchased on the Tanzanian market: International branded
versus black market products

M. Sagera, C.R. McCullochc, D. Schoderb,c,
a
Special Investigations in Element Analysis, Austrian Agency for Health and Food Safety, Spargelfeldstrasse 191, 1220 Vienna, Austria
b
Institute of Milk Hygiene, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
c
Veterinarians Without Borders, Austria

A R T I C L E I N F O A B S T R A C T

Keywords: Milk powder is a food for malnourished African children and for healthy infants of women with HIV/AIDS. High
Milk powder demand and low purchasing power has resulted in a huge informal, black market in Sub-Saharan Africa. Forty-
Element analysis three milk powder batches were analyzed for 43 chemical elements using ICP-MS One sample (2.3%) was
Heavy metal contaminated at a lead concentration of 240 µg/kg dry weight exceeding the European threshold (130 µg/kg dry
Lead
weight). Macroelement contents revealed a trend decreasing in concentration through skimmed, full cream
Iron
products to infant formulae. Concentration ranges by dry weight differed in respect of uncertainty intervals of
Baby formula
Tanzania ± 10%. Median Ca, K and P concentrations declined from 11.14 g/kg to 3.21 g/kg, 14.11 g/kg to 4.95 g/kg and
9.12 g/kg to 2.75 g/kg dry mass, respectively. Milk powder samples obtained from the Tanzanian black market
were comparable in respect of nutritional and chemical content to international branded full cream products.

1. Introduction millions of malnourished Africans, it is also recommended as a breast


milk substitute for healthy infants of women with HIV/AIDS. Alar-
The macro- and micronutrient contents of milk are known to vary mingly, some 30–50% of all HIV infections in African infants result
according to several variables, such as breed of cow, lactation status, from breast-feeding by infected mothers (WHO, 2010).
season, herd health and nutrition (Benincasa, Lewis, Sindona, & These factors are especially visible in Tanzania that is both highly
Tagarelli, 2008, Brescia, Caldarola, Buccolieri, & DelĺAtti & Sacco, populated and well served at Dar es Salaam by international shipping.
2003, Coni, Bocca, Ianni, & Caroli, 1995, Knowles, Grace, Knight, According to World Bank statistics for 2014, gross national income per
McNabb, & Lee, 2006, Sager & Hobegger, 2013). Nutrition is probably capita per month in Tanzania was US$77 and the population percen-
the most important variable because of the ease with which it can be tage living below the national poverty line, the so called poverty
modified and is dependent on a range of local infrastructure and geo- headcount ratio, was 28.2% (World Bank, 2016). Therefore, a sub-
graphic variables, such as soil, season and climate. stantial number of families cannot afford to buy officially imported
Milk is also one of the main consumable products of animal origin powdered milk at Western prices, and are forced to purchase milk
and it is particularly important for survival in overpopulated regions of powder on the informal black market (Schoder, 2010). However, due to
the world, such as sub-Saharan Africa, where meat or other sources of the international bulk buying and mixing practices of the milk powder
protein are rarely available (Schoder, Maichin, Lema, & Laffa, 2013). industry, it is very difficult to source the raw milk. This is compounded
However, its suitability for consumption rapidly diminishes if cooling by a poorly developed food surveillance system in sub-Saharan Africa,
cannot be provided. To circumvent this problem, and to make it easier which is unable to monitor food sources effectively and thereby safe-
to transport, powdering can stabilize milk. However, there are only a guard public health. These short-comings are illustrated by previous
few milk powder production plants in sub-Saharan Africa and milk studies showing that Africa was largely defenseless against the Chinese
scarcity is rectified by imported milk powder. Demand is such that up to melamine scandal; six infants died and 294,000 children developed
55% of the world’s milk powder production is sold to the African renal stones as a consequence (Schoder 2010, 2012, 2016). According
continent each year (Food and Ariculture Organisation of the United to Schoder (2010), 11% of the milk powder samples purchased in
Nations, 2013). Imported milk powder is not only a food aid for Tanzania contained melamine at dangerous levels suggesting


Corresponding author at: Institute of Milk Hygiene, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria.
E-mail address: Dagmar.Schoder@vetmeduni.ac.at (D. Schoder).

https://doi.org/10.1016/j.foodchem.2018.02.058
Received 30 June 2017; Received in revised form 6 October 2017; Accepted 11 February 2018
Available online 16 February 2018
0308-8146/ © 2018 Elsevier Ltd. All rights reserved.
M. Sager et al. Food Chemistry 255 (2018) 365–371

contaminated milk from China had made its way to East Africa, due in duplicate. These involved either nitric acid or potassium chlorate
part to lack of efficient food surveillance systems in Africa and China. (KClO3). While most of the elements can be determined by either
Therefore, given all these deficiencies, this study sought to: (i) de- method, for cationic reasons KClO3 digestion is not appropriate for K
termine the elemental composition and heavy metal contamination of and Rb. KClO3 digests are especially suitable for B, S, Si and I analyses
milk powder products purchased on the formal and informal Tanzanian and develop significantly lower internal pressures. Samples weighing
markets, (ii) check whether these products meet legal, health, and 0.25 g were digested with 3.8 ml of 65% HNO3 plus 0.1 ml of 40% HF
nutritional requirements, and (iii) compare nutritional values with and made up to 25 ml. In parallel, 1.00 g samples were digested with
Austrian reference samples. 8 ml of 7% KClO3 solution in 4.5 M HNO3 (20 g KClO3 p.a. + 200 ml
H2O + 80 ml suprapure HNO3), and also made up to 25 ml, according
2. Material and methods to Sager (2011).
A MLS 1200 mega high performance microwave digestion unit (MLS
2.1. Tanzanian milk powder supply and marketing systems GmbH, D-88299 Leutkirch) was used and programmed as follows: three
minutes at 250 W/two minutes zero/five minutes 250 W/five minutes
Tanzanian milk marketing systems can be categorized by the type of 400 W/five minutes 500 W. After cooling, the contents of the pressure
milk powder distributed and by how it is sold. Milk powder types in this bombs were made up to 25 ml in polypropylene volumetric flasks. A
study comprised: (i) branded products of international and multi- Perkin-Elmer Optima 3000 XL instrument with an axial torch was used
national companies, and (ii) illegally imported, unlabeled products sold for ICP- multi-element determinations. Matrix-matched calibrants were
openly or discretely on local black markets. Powders are sold through used for determinations following KClO3- digests. Non-metals and La-
retail and modern distribution outlets, such as: (i) supermarkets, which Ce-Y-Sc-Ti were determined in separate runs. ICP-MS measurements for
sell exclusively imported and authorized branded products, and (ii) Bi, Cd, Co, Mo, Ni, Pb, Tl, Y and the rare earth elements were performed
street vendors and micro-retailers promoting illegally imported, un- with a Perkin Elmer Sciex ELAN DRC II at 1 + 4 dilution after addition
labeled black market products. Supermarket customers in the sampled of indium (1 mg/l sample) as internal standard. Total I was measured in
regions are typically high-income earners (expatriates and nationals), a separate run as iodate after a 1 + 49 dilution with 1/80 diluted 7%
whereas street vendors and micro-retailers sell to low-income con- KClO3 digestion solution (described above) and evaluated by standard
sumers at half the usual retail price or less. addition.

2.2. Sampling and types of milk powder purchased on the Tanzanian


market 2.4. Legal requirements

Two categories of milk powder samples were selected: (i) branded The European Union has so far set thresholds for intake levels of the
products of international companies from authorized channels potentially hazardous metals lead, cadmium and mercury (European
(n = 20), and (ii) illegally imported, unlabeled products (n = 23). Commission, 2006). For many other elements, such as copper, zinc,
Branded products were purchased directly from a variety of super- chromium, iron, manganese and cobalt, levels that lead to deficiencies
markets. These products were selected on the following basis: (i) im- and chronic or acute poisonings are known, but no explicit thresholds
mediate availability, (ii) product category (milk powder-infant for- have yet been set.
mula), (iii) type of manufacturer, and (iv) production and expiry date. However, the Nutrition Societies of Germany, Austria and
Branded milk powder products could be traced to eleven international Switzerland have established various threshold values (see DACH
and multinational companies supplying the East African market (2013) for further details).
(Table 1): (i) Pharmacare, Ltd., Sandton, South Africa; (ii) Promasidor,
Ltd., Zug, Switzerland; (iii) Nestle (South Africa) (Pty.), Ltd., Randburg, 2.5. Element concentration ratios
South Africa; (iv) Daily Fresh Foods, Ltd., UK; (v) Irish Dairy Board,
Dublin, Republic of Ireland; (vi) Clover S.A. (Pty.), Ltd., Roodepoort, Due to weathering and geochemical transport of rocks, it is plau-
South Africa; (vii) Chivers Ireland, Ltd., Dublin, Republic of Ireland; sible that fractionations might occur naturally between elements with
(viii) Cow & Gate Ireland, Dublin, Republic of Ireland; (ix) Nestle Foods similar chemical properties (Wedepohl, 1995). To ascertain if this has
Kenya, Ltd., Nairobi, Kenya; (x) National Food Industries Co., Ltd., some bearing on the geographical origin of milk samples, concentration
Jeddah, Kingdom of Saudi Arabia; and (xi) Wyeth Nutritionals, As- ratios of elements were compared. Geochemically-relevant ratios are K/
keaton, Co., Limerick, Ireland. Rb and Ca/Sr. In contrast, other ratios of interest, such as Fe/Mn, Ca/
Unlabeled products (n = 23) were purchased from micro-retailers Mg, P/S and Cu/Mo, which may have relevance to bovine health and
on the local black market (Schoder, 2010, 2012, 2016). According to a nutrition, were also examined.
recent study, 300 kiosks and micro-retailers sell milk powder to low-
income consumers in Dar-es-Salaam (Schoder, 2016). The originally
packed samples were sent to the University of Veterinary Medicine, 2.6. Element comparison between Tanzanian milk powder samples and
Vienna, Austria, by air cargo, before dispatch to the analytical labora- Austrian reference samples
tory at the Austrian Agency for Health and Food Safety (AGES).
Elemental compositions of the Tanzanian milk powder samples
2.3. Digestions and inductively-coupled-plasma (ICP) multi-element were compared directly with a set of 104 Austrian reference samples.
analysis These were individual milking samples from Fleckvieh and Holstein
Friesian cows collected directly from the farm (Sager & Hobegger,
Aliquots of the milk powder samples were transferred to screw- 2013). The farms were situated within three geologically diverse re-
capped polypropylene vials and transported to the analytical laboratory gions: (i) granite-gneiss; (ii) tertiary-quaternary sediments, and (iii)
at the AGES, where the multi-element analysis was performed. Since flysch and limestone. The samples were collected in 120 ml screw-
boron and silicon were also determined, contact with glass was strictly capped, plastic vials, deep frozen and freeze-dried. They were digested
avoided. Samples were weighed into PTFE (polytetrafluoroethylene)- with concentrated nitric acid (0.25 g of sample + 3.8 ml of HNO3) and
lined pressure bombs, digestion reagents added and mixtures micro- potassium chlorate-dilute nitric acid (1.0 g of sample + 8 ml of diges-
wave-heated. tion solution) in pressure bombs by microwave-assisted heating, and
Two independent digestion methods were used and performed in made up to 25 ml in plastic volumetric flasks.

366
M. Sager et al.

Table 1
List of all tested branded milk powder and infant formula products of international and multinational companies supplying the East African market (n = 20).

N° Product Name Manufacturer Expiry date Production date Lot n° Skimmed milk Full fat cream Infant formula

a
1 Aspen™ – Nutritionals S-26/1 (Infant formula with iron) Pharmacare Ltd., Sandton, South Africa 2010–05 2008–05 502472 1
2a Nestle® Lactogen®/1 (Starter infant formula with iron) Nestle (South Africa) (Pty) Ltd., Randburg, South Africa 2009–12 2007–12 73400179L1 1
3c Wyeth® – S-26 Gold Stage 1 (Infant formula from birth to Wyeth Nutritionals, Askeaton, Co., Limerick, Ireland 2009–08 2008–02 8C295611 1
6 months)
4a Nestle® NAN®/1 (Starter infant formula with iron) Nestle (South Africa) (Pty) Ltd., Randburg, South Africa 2009–02 2007–11 7325017981 1
5a Nestle® NIDO® (Full cream milk powder) Nestle (South Africa) (Pty) Ltd., Randburg, South Africa 2010–02 2008–02 80560181 1
6a Nestle® NAN®/1 (Starter infant formula with iron) Nestle (South Africa) (Pty) Ltd., Randburg, South Africa 2010–03 2008–03 8065017981 1
7c Kerry Gold® (Full cream milk powder) Irish Dairy Board, Dublin, Republic of Ireland 2010–05 2007–05 02K/400 1
8b Cowbell® (Instant filled milk powder) Promasidor Ltd., Zug, Switzerland 2009–07 2008–04 5141A 1
9a Nestle® Lactogen®/2 (Follow-up formula with iron and Nestle (South Africa) (Pty) Ltd., Randburg, South Africa 2010–07 2008–07 82040181 SWWBFM 1
prebiotics)
10a Elite® (Fat free instant milk powder) Clover S.A. (Pty) Ltd., Roodepoort, South Africa 2009–04 NAe HO91-8-(3)-2 1
11a Aspen™ Nutritionals- S-26 Progress/3 (Growing up drink for Pharmacare Ltd., Sandton, South Africa 2010–07 2008–07 502535 1
children)

367
c e
12 Marvel (Original dried skimmed milk) Chivers Ireland Ltd., Dublin, Republic of Ireland 2009–03 NA 7268 1
13c Daily Fresh™ (Full cream milk powder) Daily Fresh Foods Ltd., U.K. 2009–12 2008–06 AM/IMP/14B 1
14c Cow & Gate®/2 (Nutritionally complete infant milk) Cow & Gate Ireland, Dublin, Republic of Ireland 2009–10 NAe 1251 1
15a Elite® (Fat free instant milk powder) Clover S.A. (Pty) Ltd., Roodepoort, South Africa 2009–03 NAe HO63-8-(3)-3 1
16b Cowbell® (Instant filled milk powder) Promasidor Ltd, Zug, Switzerland 2010–01 2008–09 4381B 1
17b Nestle® NIDO® (Full cream milk powder) Nestle Foods Kenya Ltd., Nairobi, Kenya 2009–03 2007–09 72700169 A1 1
18b Nestle® NIDO® (Full cream milk powder) Nestle Foods Kenya Ltd., Nairobi, Kenya 2009–03 2008–03 80720169 D1 1
19d Luna (Instant full cream milk powder) National Food Industries Co. Ltd., Jeddah, Kingdom of Saudi 2009–09 2008–04 104 NZMP DR 27 1
Arabia
20b Nestle® NIDO® (Full cream milk powder) Nestle Foods Kenya Ltd., Nairobi, Kenya 2009–03 2008–03 80780169 D1 1

3 9 8

a
Produced in Africa.
b
only packaged in Africa.
c
produced or packaged in Europe.
d
produced or packaged in New Zealand.
e
data not available (NA).
Food Chemistry 255 (2018) 365–371
M. Sager et al. Food Chemistry 255 (2018) 365–371

Table 2a
Main and essential trace element concentrations (mg/kg dry mass) of 43 milk powder batches collected in Dar-es-Salaam, Tanzania, East Africa.

Formal market (n = 20) Informal (African) market (n = 23)

Skimmed milk (n = 3) Full cream milk (n = 9) Infant formulas (n = 8)

Element Median Min – Max Median Min – Max Median Min – Max Median Min – Max

Ca 11,141 11,090–11,479 7666 6443–9152 3214 2820–6630 8477 7205–8867


Co 0.061 0.027–0.064 0.041 0.026–0.061 0.028 0.018–0.036 0.041 0.033–0.063
Cr 0.029 0.014–0.069 < 0.007 < 0.007–0.040 < 0.007 < 0.007–0.053 0.076 0.060–0.091
Cu 0.439 0.393–0.473 0.312 0.054–0.592 3.45 0.41–6.35 0.405 0.218–0.664
Fe 3.84 2.93–4.00 28.7 1.64–134 58.9 3.6–77.8 2.45 1.91–3.38
J 1.87 1.64–3.25 0.98 0.14–4.74 2.71 1.35–3.59 2.08 1.13–6.38
K 14,105 13,939–14,686 9545 6981–11,027 4951 3868–11,131 10,452 8988–11,386
Mg 1042 1021–1073 699 653–952 397 351–688 776 701–806
Mn 0.367 0.282–0.484 0.337 0.142–0.884 0.517 0.157–0.796 0.184 0.157–0.265
Mo 0.242 0.238–0.341 0.268 0.246–0.310 0.127 0.050–0.175 0.308 0.296–0.383
Na 3868 3717–3906 2630 2408–3731 1711 1076–2787 2777 2603–3419
P 9121 9012–9656 6055 5712–7018 2755 1888–5372 6843 5923–7411
S 3556 3542–3759 2328 861–2964 1483 1201–2024 2331 2021–2759
Zn 45.7 41.7–49.3 28.1 13.9–85.2 39.6 23.6–53.9 31.4 26.8–33.8

Table 2b
Concentration of toxic elements and elements of low physiological activity, i.e. rare earth elements (mg/kg dry mass) of 43 milk powder batches collected in Dar-es-Salaam, Tanzania,
East Africa.

Formal market (n = 20) Informal (African) market (n = 23)

Skimmed milk (n = 3) Full cream milk (n = 9) Infant formulas (n = 8)

Element Median Min – Max Median Min – Max Median Min – Max Median Min – Max

x
Ba 1.203 0.673–1.366 0.458 0.269–1.941 0.337 0.138–0.498 0.594 0.459–0.751
Cdx 0.003 < 0.001–0.003 0.002 < 0.001–0.004 0.002 < 0.001–0.007 0.004 0.002–0.008
Nix 0.08 0.04–0.13 0.03 < 0.02–0.15 0.05 < 0.02–0.17 < 0.02 < 0.02–0.05
Pbx 0.02 0.01–0.03 < 0.01 < 0.01–0.24 < 0.01 < 0.01–0.05 < 0.01 < 0.01–0.04
Al 2.2 1.6–2.7 1.85 0.5–3.8 1 0.6–2.3 < 0.5 < 0.5–1.1
B 3.53 0.83–4.12 0.78 0.27 –1.84 0.5 0.09–0.76 0.74 0.21–1.55
Be < 0.004 < 0.004 < 0.004 < 0.004 < 0.004 < 0.004–0.006 < 0.004 < 0.004
Bi < 0.04 < 0.04 < 0.04 < 0.04–0.06 < 0.04 < 0.04 < 0.04 < 0.04–0.05
Ce 0.009 0.007–0.011 < 0.002 < 0.002–0.011 0.004 < 0.002–0.010 0.002 < 0.002–0.006
Cs 0.03 0.022–0.047 0.131 0.013–0.310 0.007 0.003–0.017 0.019 0.013–0.029
Er < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001
Eu 0.0002 0.0002–0.0004 0.0002 0.0001–0.0004 0.0001 0.0001–0.0003 < 0.0001 < 0.0001–0.0002
Gd < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001–0.001 < 0.001 < 0.001
Ho < 0.0001 < 0.0001 < 0.0001 < 0.0001 0.0001 < 0.0001–0.0003 < 0.0001 < 0.0001
La 0.003 0.003–0.006 0.002 < 0.002–0.010 0.005 < 0.002– 0.014 < 0.002 < 0.002–0.004
Li 0.087 0.038–0.089 0.046 0.004–0.095 0.038 0.010–0.075 0.032 0.007–0.057
Lu < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003
Nd 0.002 0.001–0.002 0.0012 < 0.001–0.004 0.0012 < 0.001–0.005 < 0.001 < 0.001–0.001
Pr < 0.001 < 0.001 < 0.001 < 0.001–0.001 < 0.001 < 0.001–0.001 < 0.001 < 0.001
Rb 22.01 13,36–31,05 18.37 6,40–35,56 3.54 1,37–9,57 6.55 5,88–13,67
Sc < 0.03 < 0.01–0.01 < 0.03 < 0.03 < 0.03 < 0.03 < 0.03 < 0.03
Si 13.21 4.77–20.7 7.61 3.86–10.84 7.1 3.67–13.4 2.98 2.31–5.60
Sm < 0.002 < 0.002 < 0.002 < 0.002 < 0.002 < 0.002 < 0.002 < 0.002
Sr 3.09 2.56–4.52 2.79 1.93–4.37 1.56 0.82–2.95 2.69 2.28–3.03
Tb < 0.0001 < 0.0001 < 0.0001 < 0.0001 < 0.0001 < 0.0001–0.0001 < 0.0001 < 0.0001
Ti 0.19 < 0.01–0.30 0.22 0.02–0.26 0.02 < 0.01–0.13 0.11 0.10–0.15
Tl < 0.001 < 0.0002–0.0007 0.002 < 0.001– 0.006 < 0.001 < 0.001–0.001 < 0.001 < 0.001–0.001
V < 0.02 < 0.02 < 0.02 < 0.02–0.11 < 0.02 < 0.02 < 0.02 < 0.02
Y 0.002 0.001–0.002 0.002 < 0.001– 0.002 0.004 < 0.001–0.014 < 0.001 < 0.001

x toxic elements.

3. Results 3.1. Heavy metal contaminants

A total of 43 milk powder samples were collected in Dar-es-Salaam, EU regulations stipulated that cadmium intake should not exceed
Tanzania, and comprehensively analyzed for 43 chemical elements. 7 µg/kg of body weight over the course of one week, which approx-
Of the batches collected there were 20 branded products from the imates to an intake of 500 µg for an adult, assuming complete bioa-
formal market, which were manufactured and/or marketed by 11 in- vailability (European Commission, 2006). Cadmium is a toxic element
ternational and multinational companies. However, 20% of the branded and was encountered in the investigated milk powder samples over a
samples (4/20) were deficiently labeled and did not display production range from < 1 to 7 µg/kg of dry mass. Therefore in these samples it
dates (Table 1). Products from the local black market (n = 23) were was very low and comparable to Austrian reference samples (Table 2a).
completely unlabeled and packaged in simple, transparent plastic bags. A specific threshold for lead in milk has been set at 20 µg/kg fresh

368
M. Sager et al. Food Chemistry 255 (2018) 365–371

weight, corresponding to 130 µg/kg dry weight. This was exceeded in 3.4. Elemental composition of branded milk powder samples compared with
one sample, which was a full cream milk powder packaged in the UK Austrian reference samples
(branded sample number 13; Table 1) that showed a lead concentration
of 240 µg/kg dry weight (Table 2a). All other milk powder samples The elemental compositions of the branded milk powder samples
revealed lead concentrations between < 10 µg and up to 50 µg/kg dry were compared with Austrian reference samples (Tables 4a and 4b).
weight. Most of the rare earth elements, such as Be, Bi, Sc, Ti and V, Branded full cream milk powder samples had lower concentrations of
were below detection limits (Table 2a). Ca, P, Cr and Mo and higher concentrations of Fe and Sr. All other
element concentrations were either close to or below detection limits,
or were found to occur within the same ranges. In comparison, infant
3.2. Elemental composition of branded versus black market milk powder formulae contained half the concentrations of K, Mg, Mo, Na, and S, and
samples a third less Ca than the Austrian reference samples. However, con-
centrations of Cu and Fe were 10–30 times higher in baby formulae.
Branded milk powder samples of international companies for au-
thorized sale were grouped as follows: (i) skimmed milk (three sam-
ples), (ii) full cream milk (nine samples), and (iii) infant formulae (eight 4. Discussion
samples).
Macroelement (Al, B, Ba, Ca, Co, K, Li, Mg, Na, P, Rb, S) content Since cows’ milk and infant formulae are frequently the main or
revealed a trend decreasing in concentration in the order of skimmed, only source of food for infants and small children, it is essential that the
full cream products to infant formulae (see Tables 2a and 2b). Con- quality and nutritional status of these foods meet health requirements.
centration ranges by dry weight differed in respect of uncertainty in- Young children have unique nutritional requirements for growth and
tervals of ± 10%. Median Ca concentrations declined from 11.14 g/kg their digestive systems are especially efficient at absorbing essential
in skimmed milk samples, to 7.6 g/kg in (full cream samples, to 3.21 g/ elements compared with adults (WHO, 2014). Consequently, knowl-
kg for infant formulae. Similarly, K concentrations decreased from edge of reliable reference values for these elements in milk is important
14.11 g/kg to 9.55 g/kg to 4.95 g/kg for these respective samples. Mg if supplementary infant nutrition is to prove adequate.
concentrations decreased from 1.04 g/kg to 0.70 g/kg to 0.39 g/kg. P The market for milk and infant formulae is substantial. The global
concentrations decreased from 9.12 g/kg to 6.05 g/kg to 2.75 g/kg dry figure for 2014 was US$ 49.2 billion (InkedIn, 2014), and massive in-
mass (see Table 2b). ternational promotion of these products is succeeding in raising de-
The baby formulae contained more Cu, Fe and Mn, but less Mo, Si mand. This is particularly so in many low-income countries, including
and Sr than the branded full cream and skimmed milk powders. On the Tanzania, where annual sales growth is estimated at around 10%
other hand, milk powders sampled from the black market contained (Trading Economics, 2016). This contrasts with high-income countries
more Cr, Cu and I, but less Fe, Li, Mn, Rb and Si than the branded where growth is all but stagnant. Nevertheless, increased feeding of
products of international companies. However, respective concentra- these products to young children is not without concern (Piwoz, 2015).
tion ranges overlapped (see Tables 2a and 2b). Reports have surfaced about milk powder and infant formulae being
contaminated with toxic metals and environmental impurities
(Schümann, 1990). The relevance of cows’ milk for infants is also cri-
3.3. Element concentration ratios ticized, as discussed below.
Due to their low body-weights in the face of relatively high nutrient
Element concentration ratios are shown in Table 3. These data are requirements, infants are particularly sensitive to ingested con-
from samples sold on the African market and they closely resembles the taminants. Efficient gastrointestinal absorption prior to full develop-
full cream products marketed by international companies. The differ- ment of internal organs, particularly liver and kidneys, can mean that
ence is reflected in the median value for K/Rb, which was three times the effects of contaminated feed last a life-time (Oskarsson, Palminger
higher (K/Rb = 1602 versus 492) in black market samples compared Hallén, Sundberg, & Petersson Grawé, 1998). Yet, it is not uncommon
with branded full cream milk product samples. Some labeled milk for infants to be fed the same product brand daily for weeks or even
products were Fe-fortified, which was not stated on the product label months at a time.
(66.7%, 10/15, data not shown). This is revealed by the higher Fe/Mn In an effort to safeguard health, the European Union has set
concentration ratios for infant formulae (114) compared with skimmed threshold intake levels of heavy metals, including lead, cadmium and
milk powder (10.4), full cream powder (69.6) and milk powder from mercury (European Commission, 2006). In this respect, the threshold
the black market (13.08). However, the Ca/Mg concentration ratio was for lead in milk is 20 µg/kg fresh weight, corresponding to 130 µg/kg
found to be within a relatively narrow range throughout the samples dry weight. In our study this value was exceeded in one sample, which
investigated (7.0 < Ca/Mg < 15.0) and the Ca/Sr ratios were scat- was actually a legitimate full cream milk powder that was identified as
tered within a broader range (1367 < Ca/Sr < 6448). being packaged in the UK and had a lead concentration of 240 µg/kg
dry weight. Concentrations of other heavy metals were unremarkable.

Table 3
Selected weight-based element concentration proportions of 43 milk powder batches.

Formal market (n = 20) Informal (African) market (n = 23)

Skimmed milk (n = 3) Full cream milk (n = 9) Infant formulas (n = 8)

Median Min – Max Median Min – Max Median Min – Max Median Min – Max

K/Rb 633 454–1099 492 308–1632 1365 849–3398 1602 652–3306


Ca/Sr 3716 2455–4351 2584 1858–3513 2235 1625–6448 3147 1442–3655
Fe/Mn 10.4 7.94–10.92 69.6 8.29–330 114 15.0–289 13.08 9.63–38.9
Ca/Mg 10.7 10.69–10.86 10.55 8.83–11.70 8.59 7.00–15.00 11 9.82–11.80
P/S 2.56 2.54–2.57 2.73 2.37–6.80 1.93 1.47–2.65 2.84 2.57–3.45
Cu/Mo 1.81 1.15–1.99 0.84 0.19–2.28 41.1 16.0–77.6 1.32 0.42–2.18

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M. Sager et al. Food Chemistry 255 (2018) 365–371

Table 4a
Concentration Median and concentration ranges of main and essential trace elements (mg/kg dry mass) from Austrian reference samples and branded milk powder samples collected sold
in Dar-es-Salaam, Tanzania.

Lower Austria (n = 104) Full fat cream (n = 9) Infant formulas (n = 8)

Median Range Median Range Median Range

Ca 10,491 8434–13,679 7666 6443–9152 3182 2820–5659


Co 0.034 0.018–0.046 0.041 0.026–0.061 0.028 0.018–0.036
Cr 0.172 0.025–0.484 < 0.007 < 0.007–0.040 < 0.007 < 0.007
Cu 0.367 0.149–0.913 0.312 0.054–0.592 3.66 2.64–6.35
Fe 1.54 0.63–2.24 28.7 1.64–134 61.2 36.3– 77.8
J 1.78 0.65–4.77 0.98 0.14–4.74 3.06 1.35–3.59
K 10,492 8317–15,657 9545 6981–11,027 4893 3868–6944
Mg 791 646–964 699 653–952 386 351–501
Mn 0.206 0.085–0.374 0.337 0.142–0.884 0.529 0.269–0.796
Mo 0.352 0.244–0.857 0.268 0.246–0.310 0.127 0.050–0.175
Na 2724 1914–3771 2630 2408–3731 1505 1076–1895
P 7326 6178–9456 6055 5712–7018 2593 1888–4307
S 2561 2156–3498 2328 861–2964 1440 1201–1648
Zn 32.4 22.2–46.6 28.1 13.9–85.2 40.5 32.9–53.9

Table 4b
Concentration of toxic elements and elements of low physiological activity (mg/kg dry mass) from Austrian reference samples and branded milk powder samples collected in Dar-es-
Salaam, Tanzania.

Lower Austria (n = 104) Full fat cream (n = 9) Infant formulas (n = 8)

Median Range Median Range Median Range

x
Ba 0.52 0.26–0.95 0.458 0.269–1.941 0.318 0.138–0.495
Cdx 0.003 < 0.001–0.028 0.002 < 0.001– 0.004 0.002 < 0.001–0.007
Nix 0.03 < 0.02–0.185 0.03 < 0.02–0.15 0.05 < 0.02–0.17
Pbx < 0.01 < 0.01–0.07 < 0.01 < 0.01–0.24 < 0.01 < 0.01–0.05
Al < 0.5 < 0.5–1.49 1.85 0.5–3.8 1 0.6–2.3
B 0.81 0.231–1.94 0.78 0.27 –1.84 0.41 0.09–0.75
Be < 0.004 < 0.004 < 0.004 < 0.004 < 0.004 < 0.004–0.006
Bi < 0.04 < 0.04 < 0.04 < 0.04–0.06 < 0.04 < 0.04
Ce 0.003 < 0.002–0.064 < 0.002 < 0.002–0.011 0.005 < 0.002–0.010
Cs 0.013 0.003–0.084 0.131 0.013–0.310 0.006 0.003–0.017
Er < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001
Eu 0.0001 < 0.0001–0.0012 0.0002 0.0001–0.0004 0.0001 0.0001–0.0002
Gd < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001–0.001
Ho < 0.0001 < 0.0001–0.0004 < 0.0001 < 0.0001 0.0001 < 0.0001–0.0003
La < 0.002 < 0.002–0.019 0.002 < 0.002–0.010 0.004 < 0.002–0.009
Li 0.02 0.003–0.061 0.046 0.004–0.095 0.012 < 0.005–0.075
Lu < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003 < 0.0003
Nd < 0.001 < 0.001–0.023 0.0012 < 0.001–0.004 0.002 < 0.001–0.005
Pr < 0.001 < 0.001–0.008 < 0.001 < 0.001–0.001 < 0.001 < 0.001–0.001
Rb 11.1 4.6–28.6 18.37 6.40–35.56 3.28 1.37–6.40
Sc < 0.03 < 0.03–0.04 < 0.03 < 0.03 < 0.03 < 0.03
Si 7.97 0.22–20.7 7.61 3.86–10.84 6.43 3.67–13.4
Sm < 0.002 < 0.002–0.006 < 0.002 < 0.002 < 0.002 < 0.002
Sr 1.95 1.01–2.86 2.79 1.93–4.37 1.41 0.82–2.95
Tb < 0.0001 < 0.0001–0.0006 < 0.0001 < 0.0001 < 0.0001 < 0.0001–0.0001
Ti 0.115 0.04–0.176 0.22 0.02–0.26 < 0.01 < 0.01–0.13
Tl < 0.001 < 0.001–0.003 0.002 < 0.001– 0.006 < 0.001 < 0.001–0.001
V < 0.02 < 0.02–0.03 < 0.02 < 0.02–0.11 < 0.02 < 0.02
Y < 0.001 < 0.001–0.014 0.002 < 0.001– 0.002 0.005 < 0.001–0.014

x toxic elements.

Lead is a potent neurotoxin and its absorption is increased when co- (Rabinowitz, Leviton, & Needleman, 1985).
administered with milk. Exposure to the fetus and infants irreversibly Contrary to our prior concerns about hygiene at sampling sites and
affects development of the nervous system, resulting in reduced in- general milk quality in Tanzania (Schoder et al., 2013), and with the
telligence, learning disabilities (Dabeka, Fouquet, Belisle, & Turcotte, exception of the aforementioned contaminated sample, legitimately
2011) and anemia (Schümann, 1990). In comparison, studies elsewhere marketed, branded milk products of international companies and il-
have reported that typical lead concentrations in all types of infant legally imported, unlabeled products from unauthorized channels de-
formulae range from 1 to 10 ng/g when reconstituted (Dabeka, 1989); monstrated similar inorganic compositions and qualities. The elemental
although levels as high as 143 ng/g (Hafez & Kishk, 2008) and even composition of the cheapest milk powders obtained from the Tanzanian
450 ng/g (Winiarska-Mieczan & Kiczorowska, 2012) have been re- black market closely resembled those of the most expensive branded
ported. Moreover, instances of higher blood lead levels have been ob- full cream samples.
served in formula-fed infants compared with those that are breast-fed, We identified several regularities on comparing formally marketed
which may reflect contamination from storage cans or tainted tap water and black market milk samples. Black market samples were unlabeled

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M. Sager et al. Food Chemistry 255 (2018) 365–371

and packaged simply in transparent plastic bags. Nevertheless, References


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