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Chapter 9. Environmental and occupational chemicals

Chapter 9. Environmental and occupational chemicals

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Environmental and occupational chemicals



taminants may be potentially hazardous to the breast-fed infant (for reviews, see 25).

The concentrations of man-made organic chemicals in human milk are normally

more than ten times higher than in cow's milk from the same area, and commercial

infant milk formulas contain even lower levels (2, 6). Frequently, limit values established for contaminants in cow's milk are exceeded in human milk. Therefore,

new-borns and infants, whose main foodstuff is breast milk, may have a much

higher relative daily intake of these chemical pollutants than adults, and 'acceptable

daily intakes' (ADIs), tolerable daily intakes (TDIs) or provisionally tolerable

weekly intakes' (PTWIs) set by FAO/WHO for pesticides, contaminants and heavy

metals, respectively, may be exceeded (2, 6).

GLOSSARY

Abbreviation



Chemical name



DDD

DDE

DDT

Dieldrin



1,1-Dichloro-2,2-bis(p-chlorophenyl)ethane

1,1-Dichloro-2,2-bis(p-chlorophenyl)ethylene

1,1,1 -Trichloro-2,2-bis(p-chlorophenyl)ethane

1,2,3,4,10,10-Hexachloro-6,7-epoxy- 1,4,4a,5,6,7,8, 8a-octahydro- 1,4-exo-5,8-endodimethanonaphthalene

Hexachlorobenzene

1,2,3,4,5,6-Hexachlorocyclohexane

1,4,5,6,7,8,8a-Heptachloro-2,3-epoxy-2,3,3a,4,7,7a-hexahydro-4,7-methanoindene

y-HCH

Polybrominated biphenyls

Polychlorinated biphenyls

Polychlorinated dibenzo-p-dioxins

Polychlorinated dibenzofurans

2,3,7,8-Tetrachlorodibenzo-p-dioxin

Parts per billion, 10-9

Parts per million, 10-6

Parts per trillion, 10-12



HCB

HCH/BHC

Heptachlor epoxide

Lindane

PBB

PCB/Aroclor

PCDD

PCDF

TCDD

ppb

ppm

ppt



ENVIRONMENTAL POLLUTANTS IN BREAST MILK

The first environmental chemical discovered in human milk in the general population was the insecticide DDT. The average concentration found by a colorimetric

method in milk samples from 32 healthy black American women living in Washington, DC, was 130 ppb (7). During subsequent decades the development of gaschromatographic methods made detection of organochlorine contaminants much

easier and more reliable. Using this technique, Quinby et al. (8) determined DDT

and its metabolites (DDE and DDD) in human milk from the United States, and

Egan et al. (9) determined for the first time other organochlorine pesticides, including dieldrin, hexachlorocyclohexanes (HCH, BHC) and heptachlor epoxide in human milk from Great Britain.

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Peters and co-workers, investigating a mass intoxication from bread contaminated with the fungicide hexachlorobenzene (HCB) in Turkey in the late 1950s,

reported that several suckling infants were fatally poisoned by HCB received

by breast-feeding (10). In a follow-up study, the same researchers found raised

HCB concentrations in human milk from that same area 25 years after the incident

(11).

Shortly after SCren Jensen (12) in 1966 discovered that the industrial chemical

polychlorinated biphenyls (PCBs), e.g. Aroclors, were important environmental

pollutants, PCBs were determined in human milk samples from Sweden by

West66 et al. (13) and from Germany by Acker and Schulte (14). Today, PCBs are

probably the most widespread organochlorine contaminant of human milk in the

general population of industrialised societies. While the early investigations quantified the mixture of PCB congeners, the most recent studies may quantify the single PCB congeners including the most toxic, so-called co-planar PCB congeners

(15).

The first detection of organophosphorous pesticides in human milk was made in

Taiwan by Yeh et al. (16), who found an average concentration of 1.9 ppm of

malathion (used as a DDT substitute in Taiwan) in whole milk; this value was 50

times that of DDT in the same samples.

Brilliant et al. (17) detected polybrominated biphenyls (PBBs) in most human

milk samples analysed from the State of Michigan (USA) after the 1973 pollution

incident, in which animal feed was accidentally contaminated with PBBs, mainly

hexabromobiphenyls.

Rappe et al. (18) were the first scientists who discovered 'dioxins' (chlorinated

dibenzo-p-dioxins and chlorinated dibenzofurans) in human milk from European

countries. 'Dioxins' included the extremely toxic compound 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) determined in concentrations of 1-2 ppt. TCDD is wellknown from the 'Seveso' accident on 10 July 1976 in a chemical plant (ICMESA),

located near the town of Seveso in northern Italy. Shortly after the explosion, up to

7.9 ppb of TCDD was detected in milk from cows grazing in contaminated zones

(19). TCDD concentrations in human milk fat from the polluted area were 2-28 ppt

with an average of 13 ppt (20).

Very recently the persistent and bioaccumulating 'nitro musks', which are

widely used as fragrances in cosmetics and detergents, have been detected (up to

0.3 ppm) in human milk from the northern part of Germany (21).

Other potentially hazardous environmental chemicals have been detected in human milk, for instances, pentachlorophenol (22), traces of nitrosamines (23), and

polycyclic aromatic hydrocarbons (PAHs) (24) and no doubt others will be discovered in the future. Pellizzari et al. (25) identified about 200 different volatile

chemical compounds in 12 samples from four urban areas in the United States, indicating a much broader chemical contamination of human milk from the general

population than had previously been expected (Table 1).

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Environmental and occupational chemicals

TABLE 1



Volatile chemicals identified in at least 7 of 12 samples of human milk from 4 urban areas of the USA



(25)



Aliphatic

hydrocarbons



Cyclic

hydrocarbons



Halocarbons



Others



Pentanes

Hexanes

Heptanes

Octanes

Nonanes

Decanes



Benzene

Toluene

Xylene

Ethylbenzene

Styrene

Limonene



Methylenechloride

Methylchloroform

Chloroform

Trichlo~oethylene

Perchloroethylene

Dichlorobenzene



Isopropylalcohol

Acetone

Acetophenone

Pentanal

Hexanal

Carbondisulfide



ACCUMULATION OF POLLUTANTS IN BREAST MILK

Lipophilic, un-ionised organic chemicals readily penetrate the cellular barriers between blood plasma and breast milk and concentrate in the fat globules. In this

way, chemicals can be transferred and attain significant concentrations in human

breast milk, if exposures are either periodically high or life-long (26, 27).

Periodically high exposures to lipophilic chemicals, e.g. organic solvents, halocarbons and pesticides, may occur in some occupations, but are rare in the general

population apart from a few incidences of mass intoxication. Of more relevance for

the general population are life-long exposures to low levels of certain lipophilic and

metabolically persistent environmental chemicals, such as the organohalogens DDT

and PCBs, to which practically everyone is exposed, either directly or through food

chain bioaccumulation (27).

In mammals these chemicals are efficiently absorbed through the skin, lungs and

gastrointestinal tract, and they mainly bind to very low density lipoproteins

(VLDL) in the blood. As they are only slowly or even negligibly metabolised by

and eliminated from the body, most absorbed material is retained unchanged, and

thus the body burden gradually increases. The main storage is in the adipose tissue

(28).

In females, pregnancy and lactation change the accumulation and distribution of

lipids in the body (26). Lipids and lipophilic contaminants are transferred into

breast tissue from adipose tissues. A lactation period mobilises 10-20% of fat deposits in the body (29). In Germany it was estimated that a women during her pregnancy and delivery loses about 16 kg body weight (30). Lactation will in practice

be the most important route of excretion for bioaccumulating, lipophilic chemicals

(17). Experiments with lactating mice have indicated that essentially the entire

body burden of persistent PCBs and HCB may be eliminated and transferred to

nursing offspring by 20 days postpartum (31, 32, 26).

Under normal circumstances, the concentrations of organohalogens in human

milk fat largely reflect the amounts in adipose tissue, and daily intakes of the

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Environmental and occupational chemicals



chemicals during lactation are in general without great influence on the concentrations in breast milk (24, 33, 34).

CONCENTRATIONS AND TRENDS OF ENVIRONMENTAL CHEMICALS IN

HUMAN MILK

During the past two decades, many scientists have reported contamination of human milk by environmental chemicals. Investigations differ greatly in purpose,

scope, design, size, selection of milk donors, sampling methods and chemical

analysis. Most studies involve too few samples and mothers to make any real conclusions about the origin of the contamination. Some studies ignore factors that are

known to affect the concentrations of contaminants in human milk (see 'Factors

that affect the level of contamination', p. 686), and other studies lack sufficient

analytical quality control.

Differences in the method of assay may substantially affect the results, especially in the case of PCBs and dioxins. Therefore, it is not surprising that published

data, even within the same country or district, may differ greatly, and comparisons

of the findings of different research groups should be interpreted with great caution. With this reservation, some recent results of average DDT, PCB and 'dioxins'

(PCDDs + PCDFs) concentrations in human milk fat obtained from individuals

living in various countries are selected and shown in Figs. 1-4.

Typically, the concentrations of DDT are higher in samples from developing

countries with current or recent usage of persistent pesticides. Levels are extremely

high in areas of these countries where DDT is spayed The concentrations of PCBs

and dioxins are higher in samples from industrialised countries, whereas these



FIG. 1 Average DDT + DDE in human milk fat from European countries. The number of individuals from whom

samples were taken is shown in parentheses.



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Environmental and occupational chemicals



FIG. 2 Average DDT + DDE in human mild fat from countries outside Europe. The number of individuals from

whom samples were taken is shown in parentheses.



chemicals often are not detectable in samples from developing countries. If only a

few PCB peaks are used for the chromatographic quantitation, then PCB levels are

approximately twice as high.

The trends in average DDT, DDE, and PCB concentrations in human milk dur-



FIG. 3 PCB in human milk fat: Average concentrations. The number of individuals from whom samples were

taken is shown in parentheses.



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Environmental and occupational chemicals



FIG. 4



Average dioxin toxicity equivalents (I-TEQ) in human milk fat.



ing more than a decade in Sweden are illustrated in Fig. 5. The samples are from a

milkbank in Stockholm, and the contaminants were determined by the same laboratory and similar methods (35, 75).

Concentrations of DDT and its metabolite DDE decreased throughout the period



FIG. 5



Trend of DDT, DDE and PCB levels in human milk from Stockholm.



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Environmental and occupational chemicals



studied, DDT faster than the more persistent DDE. The levels of PCBs increased in

the first years, followed by a weak downward trend. Investigations from other

European countries have not indicated a clear decline of PCB concentrations in

human milk (24, 29), if the same analytical method is used It is worth noting that

the methods of chemical analysis that are most popular nowadays should give

lower values than those that were used some years ago (76).

Heavy metals may also contaminate human milk. Concentrations direct toxic to

the suckling infant (<200 ppb mercury in whole milk) were, for instance, observed

in connection with the tragic 1972 mercury poisoning episode in Iraq (77).

Some recent data on average concentrations of lead, cadmium and mercury from

different countries are shown in Figs. 6-8, respectively. Again, some of the differences may be explained by the different analytical methods used

FACTORS THAT AFFECT THE LEVELS OF CONTAMINATION

Several factors may influence the actual amounts of environmental chemicals in

individuals. These include: (a) fat content of breast milk, (b) sampling time in lactation, (c) maternal age, (d) maternal parity and history of delivery, (e) maternal

weight, (f) maternal origin and residence, (g) maternal diet, (h) seasonal differences,, (i) maternal smoking, (j) maternal use of biocides, (k) maternal use of cosmetics, and (1) maternal occupation. Some of the published investigations include

too few mothers/samples that the differences found were not statistical significant.



FIG. 6 Lead in human milk average concentrations. The number of individuals from whom samples were taken

is shown in parentheses.



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Environmental and occupational chemicals



FIG. 7 Cadmium in human milk average concentrations. The number of individuals from whom samples were

taken is shown in parentheses.



Fat content of breast milk and daily fluctuations

The average concentration of fat in breast milk is around 3-4% but varies between

individuals and fluctuates within an individual during a feed, during a day, and

from day to day (96). Since most residues are lipophilic and associated with the

milk fat, the concentration of residues will also fluctuate.



FIG. 8 Mercury in human milk average concentrations. The number of individuals from whom samples were

taken is shown in parentheses.



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Environmental and occupational chemicals



Mes and Davies (97) reported 5-fold differences of PCB concentrations in whole

milk during one feed, or during the day in single donors. There was a tendency to

higher concentrations later in a feeding period. The same trend was reported by

Wilson et al. (98) and Barnett et al. (99) with DDT. When the data were corrected

for milk fat content, however, very small or no differences were observed Therefore, comparison of results of different investigations of lipophilic contaminants

must take into account variation in milk fat.

Pluim et al. (100) have recently found significant higher dioxin concentrations in

milk fat from mothers milk collected in the evening compared with collection in

the morning.

Sampling time in lactation

During the lactation period the fat% in breast milk decreases (101). The concentrations of organohalogens are generally lower in whole colostrum (fat deficient) than

in mature milk; but the quantities are higher in colostmm fat than in mature milk

fat (102). The content of heavy metals are, however, higher in whole colostrum

(81).

There appears to be a tendency towards a gradual decrease of organochlorine

residues in both whole mature milk and milk fat during the first 6-12 months of

lactation, especially if the concentration of the residues at the start of breast-feeding

is relatively high. DDT and HCB in milk fat from 12 Austrian donors decreased to

one-third of the initial level during about 10 weeks, and reached the current Austrian limits for cow's milk (1 and 0.5 ppm, respectively). The decrease continued to

a lesser degree during the following weeks (103). Earlier, Acker and Schulte (104)

reported a 30% decrease of DDT in human milk fat during the first 3 months of

lactation. In an investigation of DDE and PCBs in milk fat from an occupationally

exposed Japanese woman, concentrations of PCBs gradually decreased from about

15 ppm to less than 5 ppm after a year. In the same period, the DDE concentration

decreased from 4 to 1 ppm in milk fat (105). In Canada, Mes et al. (106) reported a

small but statistically significant decrease of/3-HCH, HCB, DDE and DDT in milk

fat during lactation. Rogan et al. (48) reported a 20% and 40% decrease in DDE

and PCB in milk fat from the United States in 6 and 18 months, respectively. In

Norway, PCB levels in milk fat decreased 30% in 4 months (107). Also dioxin

levels may decrease up to 50% in 1 year (71,108).

The heavy metals lead and cadmium, also show a decrease in human mature

milk concentration with lactation time (81, 91,109, 110).

Maternal age

The daily rate of elimination from the body of persistent organohalogens is generally less than the daily uptake rate. Increasing accumulation by age of these sub688



Environmental and occupational chemicals



stances in adipose fat (111) and in blood serum (112, 113) is therefore not surprising. In studies involving a very large number of samples Rogan et al. (48) reported

20-30% lower levels of DDE and PCB in 16-24-year-old compared with 30-41year-old mothers, and Ehrensdorfer et al. (29) found a gradually increase of 50% of

DDT and PCB from the year 20 to 45. Dioxin concentrations in milk fat also increased significantly with age (114).

In many earlier human milk studies there was no clear relationship between maternal age and the concentration of residues in human milk, possibly because of low

sample size, the relative youth of women giving birth and because of confounding

factors such as parity (115).



Maternal parity and history of delivery

Since lactation is the most important route of excretion of persistent organohalogens, previous lactations are likely to deplete the deposits. Indeed most studies

confirm that the concentrations of DDT/DDE (38, 48, 49, 66, 116-125, 127), PCBs

(48, 66, 107, 121-125, 127), fl-HCH (116, 128, 127), y-HCH (129), HCB (128),

dieldrin (130) and dioxins (71) in human milk or milk fat decrease with parity.

Normally, significant differences first occur after the second birth.

Mothers giving birth to twins (or for other reasons having an increased milk production) excrete a relatively higher amount of DDT overall (131). Women undergoing premature delivery and stillbirth were found to excrete more DDT in their milk

than those undergoing full-term, normal delivery (132).



Maternal weight

In general, slim persons have less fat deposits and higher concentrations of DDT

and PCB in adipose fat tissues (57, 104, 133-135). In whole human milk, Polishuk

et al. (133) observed higher concentrations of DDT, y-HCH, dieldrin, heptachlor

epoxide and PCBs in mothers who weighted less than 63 kg, compared to mothers

who weighed more than 72 kg. A similar association with DDT in whole milk was

found by Knoll and Jayaraman (117), and with dieldrin, heptachlor epoxide and yHCH in whole milk, and dieldrin and heptachlor epoxide in milk fat by Miller et al.

(102). Other investigations have not observed the influence of maternal weight.



Maternal origin and residence

Investigations in the USA and Brazil have suggested a racial factor in human milk

contamination. In both countries, mothers from black population groups had higher

DDT concentrations in their milk than had white mothers (123, 136). It is more

likely that these differences are attributable to socioeconomic factors as was observed by Davies et al. (137) who assessed the body burden of DDT.

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Environmental and occupational chemicals



In many industrial countries, female immigrants from less developed countries

may have far more DDT and less PCBs in their breast milk than have native citizens (40, 138-142). These findings may be explained by higher exposure to DDT

and lower exposure to PCB's in the less developed countries, and the persistence of

these chemicals in body fat. A investigation of 33 mothers who emigrated from

Turkey to Germany showed a significant positive correlation between PCB concentration in milk fat and residence time in their new country (143).

In general, mothers from urban areas have higher DDT concentrations in their

milk than do mothers from rural areas, as long as DDT has not been used commercially in the area (58, 119, 144, 145). On the other hand, DDT may reach enormously high concentrations in rural and agricultural areas, where the pesticide is

still in use (49, 53, 55, 99, 146).

PCB and dioxin concentrations are also higher in urban and industrial areas than

in rural areas (129, 147, 148). The principal source may be air pollution. In a Canadian study, the highest concentration of PCBs was detected in milk from a

woman who had lived close to a municipal waste incinerator for 5 years (129). In

the Northem Canada, Dewailly et al. (149, 150) found that Inuit women had 2-10

times more PCB (including co-planar congeners) and dioxins in their milk than

Caucasian women. The reason is the high intake of contaminated marine mammals

(see later). In Germany and Brazil, the concentrations of fl-HCH were highest in

milk from mothers who lived in rural areas (58, 151).

Regional differences in both organochlorine pesticides and PCBs in human milk

have been observed in Sweden (152). The concentrations of all residues were generally lower in the northem and less densely populated parts. DDT and fl-HCH

concentrations in milk from mothers living in the capital, Stockholm, were about

the same as those from Lund, a southern, less-industrialised university city. The air

fallout of PCBs is greater in southern Sweden, because of long-range carriage from

central Europe. Conceming dioxins Ftirst et al. (71) reported no difference between

breast milk from urban and rural areas.

Area of residence also has an important influence on the heavy metal content of

human milk. Breast milk from an area of Austria with high traffic density had a

50% higher lead content than that from rural areas (153). In Poland, both cadmium

and lead in human milk were significantly higher in industrial compared to agricultural areas (84). In Mexico City close to a smelter, extremely high lead concentrations were found in blood and breast milk samples (154). Lead concentrations in

milk from an industrial city in Romania were more than 10 times higher than those

from a pollution-free town (155).

Maternal diet



Apart from direct exposure to chemicals, ingestion of contaminated foodstuffs is

often recognized to be the main source of persistent environmental chemicals in the

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