Longitudinal and contemporaneous manganese exposure in apartheid-era South Africa: Implications for...

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International Journal of Paleopathology 8 (2015) 1–9

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International Journal of Paleopathology

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esearch Article

ongitudinal and contemporaneous manganese exposure inpartheid-era South Africa: Implications for the past and future

atherine A. Hessa,b,∗, Martin J. Smitha, Clive Truemanc, Holger Schutkowskia

Faculty of Science and Technology, Bournemouth University, Talbot Campus, Fern Barrow, Poole BH12 5BB, UKDepartment of Environmental Health, Bloomberg School of Public Health, Johns Hopkins University, 615 N. Wolfe St., Baltimore, MD 21205, United StatesOcean and Earth Sciences, University of Southampton, National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK

r t i c l e i n f o

rticle history:eceived 17 February 2014eceived in revised form 8 September 2014ccepted 21 September 2014

eywords:anganeseuman exposureouth Africaone concentration

a b s t r a c t

Manganese is a potent environmental toxin, with significant effects on human health. Manganese expo-sure is of particular concern in South Africa where in the last decade, lead in gasoline has been replaced bymethylcyclopentadienyl manganese tricarbonyl (MMT). We investigated recent historical levels of man-ganese exposure in urban Gauteng, South Africa prior to the introduction of MMT in order to generateheretofore non-existent longitudinal public health data on manganese exposure in urban South Africans.Cortical bone manganese concentration was measured by inductively coupled plasma mass spectrom-eter in 211 deceased adults with skeletal material from a fully identified archived tissue collection atthe University of Pretoria, South Africa. All tissues came from individuals who lived and died in urbanGauteng (Transvaal), between 1958 and 1998. Median Mn concentration within the sampled tissueswas 0.3 �g g−1, which is within reported range for bone manganese concentration in non-occupationallyexposed populations and significantly below that reported in individuals environmentally exposed toMMT. No significant differences were seen in bone Mn between men and women or in individuals of dif-ferent ethnicity, which further suggests environmental, as opposed to occupational exposure. There were

. Introduction

Manganese is both an essential trace element and a potentoxin in humans. Exposure to toxic levels of manganese gen-rally occurs in industrial regions as a result of smelting andining activities and through occupational exposure, as well

s through contaminated ground water (Groschen et al., 2008;ichalke et al., 2007; Nelson et al., 2012). In many regions,

uman exposure to manganese is the result of inhalation of

ound added to gasoline as an anti-knocking agent and releasednto the air in vehicle exhaust (Walsh, 2007). Manganese affects

∗ Corresponding author at: Department of Environmental Health, Bloombergchool of Public Health, Johns Hopkins University, 615 N. Wolfe St., Baltimore, MD1205, United States. Tel.: +1 4435625300.

E-mail address: chess5@jhu.edu (C.A. Hess).

human health at the acute level and the chronic, sub-clinical level(He and Niu, 2004). The biological effects of manganese expo-sure are primarily neurological, though other organ systems suchas the liver can be affected as well (Butterworth et al., 1995).Acute exposure is generally characterized by severe neurologicaldisturbance and with Parkinson’s like pathology (tremors, lossof coordination, motor skill deficits) whereas chronic exposurecan result in milder motor skills deficits and mood disturbances(Bouchard et al., 2007, 2011; Bowler et al., 1998; Mergler et al.,1999; Roels et al., 2012). Manganese affects neurological devel-opment and the central nervous system by interfering with thefunction of the neurotransmitter dopamine (Aschner and Aschner,1991; Butterworth et al., 1995; Normandin and Hazell, 2002; Verity,1999). Manganese accumulates in the central nervous system

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o children’s neurological development is under debate (Riojas-odríguez et al., 2010; Sharma, 2006). Recent research suggests thatanganese levels commonly found in tap water, approximately

4 �g/L, are enough to cause a reduction in IQ (Bouchard et al.,011). Manganese is also known to affect sight and can cause nightlindness in exposed children (Afridi et al., 2011).

The purpose of this research is twofold. Firstly to investi-ate historical exposure to manganese from a bioarchaeologicalnd anthropological framework and secondly to establish base-ine exposure data, which may inform future investigations into

anganese exposure in urban South Africans. In the first instance,he relative lack of environmental data for the late 20th centuryncourages a bioarchaeological approach to gathering such data.uman skeletal tissue serves as an excellent biological repositoryf many metals and is a useful matrix for investigating environ-ental exposures in historical populations and to identify historical

ealth issues. The primary aim is to determine whether manganesexposure during this time period followed the same exposure pat-erns as other toxic elements, such as lead, which vary significantlyccording to apartheid-designated racial groups. Secondly, from aublic health perspective, this research addresses the lack of dataegarding manganese exposure in an urban South African pop-lation prior to the introduction of MMT and to compare boneanganese concentration in these individuals with individuals in

ther industrialized regions both with and without MMT exposure.n addition, the exposure pattern identified here provides valuablenformation regarding manganese exposure which can be used tonform future exposure patterns within the urban population ofauteng, South Africa.

This paper uses terminology not frequently employed in anthro-ology or bioarchaeology. Throughout, we refer to individual racend individual South Africans as either black or white, as opposed toeferring to ethnicity or ancestry. Race, in this instance, is a proxy forocial, cultural and economic differences within the South Africanopulation. We use this terminology for two reasons. Firstly race,s a social, but certainly not biological construct, existed in a veryoncrete way during the apartheid era in South Africa, and thendividuals included in this study were separated and segregatedn every aspect of life according to their government-designatedacial category of either black or white. In addition race, as a socio-ultural construct (and distinct from biological or genetic ancestry)as been shown to have a profound impact on health and healthutcomes worldwide and is an important factor in the social deter-inants of health and environmental epidemiology (Dressler et al.,

005; Gee and Devon, 2004; Gravlee, 2009; Gravlee and Dressler,005; Gravlee et al., 2005; Hicken et al., 2012; Williams and Collins,001). As such, race is often used as a categorical variable in epi-emiological studies as it is here, and the terms “black” and “white”re common categorical designations.

.1. Manganese biomonitoring and toxicokinetics

Manganese is generally biomonitored in blood, however hair,ail and bone manganese are indicators of chronic exposure (Smitht al., 2007; Sriram et al., 2012; Zheng et al., 2011). The relationshipetween blood and urine manganese and airborne manganese isnclear, however blood manganese concentrations in individualsorking in areas with high levels of airborne manganese do tend

o be significantly higher than those in low-airborne manganesereas (Lucchini et al., 1999). The relationship between blood man-anese and bone manganese is unknown and it is difficult to makeirect comparisons between bone and blood measurements in

of Paleopathology 8 (2015) 1–9

to measure change across time and across a given population.Manganese is a bone-seeking element, with approximately 40%of manganese stored in bone, making bone useful as a matrix forstudying past exposure (Arnold et al., 2002). To date, studies ofbone manganese concentrations are few in number, but the use ofbone tissue as an alternative biomonitor of manganese exposure isgaining acceptance (Arnold et al., 2002; Aslam et al., 2008; Pejovic-Milic et al., 2009; Zheng et al., 2011). In bone tissue manganese isthought to follow the same kinetic pathway as iron, and whilst itis often included in trace element studies of bone tissue, little iswritten about manganese-bone interaction and how bone man-ganese concentration can be interpreted. Moreover, manganeseis essential in bone remodelling as it regulates the formation ofthe osteoid matrix a process dependent on glycosyltransferase,a manganese-dependent enzyme (Gonzalez-Perez et al., 2012).Decreased rates of bone remodelling are evident in manganese-deficient animals and decreased serum manganese concentrationsevident in osteoporotic, postmenopausal humans (Odabasi et al.,2008; Strause and Saltman, 1987; Strause et al., 1987). Manganeseregulates the formation of the osteoid matrix and the processis dependent on glycosyltransferase, a manganese-dependentenzyme (Gonzalez-Perez et al., 2012).

1.2. Manganese in South African environment

Since the 1990s, MMT has been added to petrol as an anti-knock and octane enhancer as a replacement for tetraethyl lead(Batterman et al., 2011; Forbes et al., 2009; Röllin et al., 2005). SouthAfrica began replacement of lead in petrol with MMT in 2005 andit is unclear as to the effect of this action on manganese exposurein the South African population. There were no published studiesof manganese exposure in the South African population prior to2006 with one exception: Myers et al. (2003) study of manganesebiomarkers in a population of highly exposed ferroalloy smelters.

The use of MMT as a gasoline additive has been controversial,despite its widespread use. Much like its predecessor lead, MMTis emitted into the atmosphere as particulate matter where it isreadily bioavailable to humans (Aschner and Aschner, 1991; Levyand Nassetta, 2003; Lucchini et al., 2009; Spangler, 2012). There issufficient evidence that inhaled manganese is particularly damag-ing to human health. Clinical manganese neurotoxicity is evidentat airborne manganese concentrations greater than 1.0 mg/m3,indicating that inhaled manganese affects the body differentlythan ingested manganese, though the mechanism is still unclear(Santamaria and Sulsky, 2010). It is clear, however, that inhaledmanganese adversely affects neurological, pulmonary and repro-ductive function in exposed adults and children (Boyes, 2010).

Though the data on environmental manganese concentrationsin South Africa prior to the mid-1990s are almost non-existent,Formenti et al. (1998) conducted PIXE analysis on urban aerosolsin Soweto from 1982 to 1984. They conclude that atmosphericmanganese in Soweto was likely due to manganese smelting activ-ities near Johannesburg. The authors also note that the presence ofmanganese in the atmosphere was intermittent and dependent onsoutherly wind, which would not have been often. With regards tothe substantial mining activities in the region, aerosol monitoringof a Transvaal goldmine conducted in the late 1980s found negli-gible manganese concentrations in dust resulting from any miningactivities (Annegarn et al., 1987). Prior to the use of MMT then,the most likely source of manganese in urban Gauteng would havebeen smelting as it used extensively in the production of steel,and ferromanganese alloys. Gauteng has been characterized by

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Table 1Number of males and females, black and white South Africans in sampled remains.

Black White

innitt, 2010). Recent analysis of the trace element constituentsf fly ash, soil and plants near coal-fired power plants indicatesevels of manganese in soil and plants that exceed the Worldealth Organisation and the Food and Agricultural Organisation’s

ecommendations regarding maximum manganese concentrationsAyanda et al., 2012; Okedeyi et al., 2014).

.3. Social and physical geography of the Johannesburg/Pretoriaegacity

The social geography of the South African landscape duringpartheid was unique. The Group Areas Act of 1950 brought abouttrict rules regarding racial segregation within the urban environ-ent. Under the Group Areas Act, black South Africans who lived

n urban areas were forced into suburban townships. The Groupreas Act ensured no mixing of races in neighbourhoods and com-lete separation of races in regards to residence, shopping, markets,ervices, and public amenities such as parks. Black South Africansn both Pretoria and Johannesburg were expected to live in town-hips outside of the city, hostels, if they were men migrating in from

rural homeland. Many black South Africans also lived in infor-al squatter camps that appeared around the cities towards the

nd of apartheid, as more individuals migrated from rural areas inearch of work (Christopher, 2005; Richards et al., 2007). It has beenstimated that by the 1980s nearly 1.5 million intra-urban com-uters moved between townships and urban centres daily (Khosa,

998). In Pretoria, an estimated 400,000 labourers travelled into theity core each day, with an average commuting distance of 52 kmKhosa, 1998). The result was a substantial degree of traffic conges-ion and accompanying pollution in and around the urban core inhese cities (Beavon, 2001). The movement of black South Africanso the urban periphery served to locate them closer to industrialnd mining activities (Hattingh and Horn, 1991).

The physical geography of urban Gauteng (formerly Transvaal)s marked by the proximity of the two cities, often referred to as

“megacity” (defined as having >10 million residents) and is theargest urban area in Africa (Fig. 1) (Lourens et al., 2012). The megac-ty is located within close proximity to the industrial regions ofhe Highveld to the Northeast of Pretoria and the Vaal Triangle tohe South of Johannesburg, both regions of intense metal and coal

ining and industry (McCarthy, 2011; Rogerson, 1990; Terblanchet al., 1992).

Given urban residential patterns and heavy industry as the mostikely source of environmental manganese we expected to seeigher rates of manganese among black South Africans than amonghite South Africans. An investigation of bone lead concentrationas conducted on the same collection (Hess et al., 2013) and sig-ificant differences in bone lead were apparent among individualsf different ancestry. Similarly, analysis of cadmium and arseniclso differ according to ancestry within the same sampled remainsHess, 2013). The variation in exposure to these elements is ascribedo Apartheid policies, which segregated the South African popula-ion along strict racial lines. Thus despite residing in the same cities,nd in some cases in relatively close proximity within the urbanandscape, individuals classed as either black or white accordingo the 1950 Population Registration Act experienced very differentates of exposure to inorganic pollutants.

. Materials and methods

Cortical bone samples were taken from the skeletal remains of

nalysis is permitted. A small number of remains were sampled

Males 130 35Females 49 0

from the Raymond Dart Bone Collection held at the University ofWitwatersrand. Both collections are fully identified, with individ-ual age, ancestry, sex and cause of death accurately recorded. Thedemographic composition of the Pretoria Student Bone Collectionis the same as for the Identified Bone Collection (L’Abbe et al., 2005).Remains in this collection were never subject to burial and as suchthere are no post-mortem diagenetic complications which maycompromise the analytical results. The skeletal remains are thoseof individuals who died in the Pretoria area between 1943 and 2012and whose bodies were either unclaimed by relatives or donated. Inthe former case, unclaimed bodies become the property of the Uni-versity of Pretoria to be used for teaching and research, subject tothe South Africa Human Tissues Act of 1983 (L’Abbe et al., 2005). Thecollection consists of individuals who range in age from neonates to95 years of age. The terms “black” and “white” are used in this papersolely in reference to socioeconomic and cultural group affinity, andfollow the racial classification of skeletal remains in the collection(L’Abbe et al., 2005). We have retained this terminology becauseit is the basis on which the individuals comprising the collectionwould have been residentially, economically and legally separatedduring life, in accordance with the South African Population Reg-istration Act of 1950. The predominant demographic within thecollection is black South African males. This is largely to do withoverall demographic patterns within South Africa (Byerlee, 1974;L’Abbe et al., 2005; Smit, 2001). The Raymond Dart Collection ishoused at the University of Witwatersrand, School of Medicine andis similar in demographic composition to the Pretoria Collection.Skeletal remains in the Dart collection date from 1928 (Dayal et al.,2009). Only 12 of the femora included in this study are from theDart collection. The demographic profile of the sampled skeletalremains is given in Tables 1 and 2.

It was not possible to include white females in this study dueto their scarcity within the fraction of the collections available fordestructive analysis. With this exception however, the demogra-phy of the subsample is representative of the overall demographicmakeup of the collection, with regards to age, sex and ancestry.Black females comprise 23% of the sampled remains and makeup 16% of the total collection. The mean age for black females inthe collection is 47.4, and is 48.2 in the sampled remains. Whitemales comprise 16% of both the total collection and the sampledremains. The mean age of white males in the whole collection is66.5 and the mean age in the sampled remains is 66. Black malescomprise 60% of the complete collection and comprise 60% of thesampled remains. In terms of age, the mean age of black males inthe complete collection is 53.9, and is 51.2 in the sampled remains.

Demographic information such as age, sex and ancestry weretaken directly from cadaver records associated with each indi-vidual. Individual ancestry was presented in racial groups andindividuals were classified as either black or white. These recordsare based on information provided by the admitting hospital at thetime of death and based on the Population Registration Act, whichclassified South African individuals by race (Christopher, 1990). Cityrefers to the city in which the admitting hospital is located and isused as a proxy for residential history.

Analytical methods follow the procedure described previously

4 C.A. Hess et al. / International Journal of Paleopathology 8 (2015) 1–9

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ig. 1. The Johannesburg and Pretoria megacity (1:50,000). Pretoria and Johannesbf Gauteng (formerly Transvaal).

OpenStreetMap contributors.

ubject to nitric acid digestion. In order to compare differentong bones effectively, six long bones were taken from each of5 individuals and bone element concentrations measured. Noignificant differences in intra-individual bone Mn concentration

able 2emographic breakdown of sampled remains. Includes age and residence by ancestry an

Mean age Median age SD Min. age Max. age

All 53.01 55 16.06 20 95

White males 66 67 13.1 42 95

Black females 48.2 46 14.67 25 80

Black males 51.2 50.5 15.28 20 80

mprise one large “megacity”, with Pretoria to the North in the Northeast province

were found (Hess, 2013). Analysis was conducted at the Universityof Southampton Geochemistry Class 100 Clean laboratory at theNational Oceanography Centre Southampton. Samples were ana-lyzed by ICP-MS (Thermo Scientific XSeries 2). Certified reference

d sex.

Pretoria (n) Johannesburg (n) Rural (n) Unk. (n) Total (n)

153 39 6 13 21117 6 2 10 3539 8 1 1 4997 25 3 2 127

C.A. Hess et al. / International Journal of Paleopathology 8 (2015) 1–9 5

Table 3Descriptive statistics for bone Mn concentration in �g g−1 within the sampled remains.

Group N Mean Mn Median Mn SD Minimum Maximum

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129 0.48

White males 35 0.44

Black females 44 0.41

aterial, NIST SRM 1486 Bone Meal was used for method vali-ation. Ten 0.1 g samples of reference bone meal were analyzedlongside analytical samples. Mean Mn recovery was withincceptable range.

Bone Mn is not normally distributed and in all cases, non-arametric statistical tests are used. In the case of multipleomparisons, Bonferroni’s correction is applied (˛/n).

This research was approved by the Bournemouth University Eth-cal Review Committee and the University of Pretoria, Departmentf Anatomy. In addition, the project met all requirements set byhe UK Human Tissues Act (1994) governing the use of human tis-ues for research and bone samples were imported into the UK andnalyzed in accordance with the Act.

. Results

Descriptive statistics for bone Mn concentration in the sam-led remains are given in Tables 3 and 4. Bone Mn concentration

s not normally distributed. There is no significant difference inone manganese between any of the demographic groups amonghese remains. Black females, white males and black males have

edian bone manganese concentrations of 0.31 (SD = 0.31), 0.25SD = 0.07) and 0.32 (SD = 0.56) �g g−1 respectively. There is no sig-ificant difference in bone Mn concentration between black andhite South Africans (Mann–Whitney U = 3263, p > 0.05). Amongales only, there is no difference in bone Mn between black andhite males (U = 2156, p > 0.05). Between black males and females,

here is also no difference in bone Mn (U = 3114.5, p > 0.05). Betweenlack females and white males, there is no significant difference inone Mn (U = 1317, p > 0.05).

There is significant difference in median bone Mn across timen all individuals (H(3) = 9.50, p < 0.05). Initial analysis reveals thatndividuals who died between 1990 and 1998 had significantlyigher bone Mn concentrations than individuals who died between960 and 1969 (Fig. 2). Subsequent pairwise comparisons with Bon-erroni’s correction (0.05/4) confirm that individuals living in the990s had significantly higher bone Mn concentrations than in the960s, however no other decades differed. When individual demo-raphic groups are separated however, this trend is not significant.n black females, bone Mn appears to be greatest in individuals whoied between 1970 and 1979, however a Mann–Whitney test withonferroni correction (0.05/4) indicates none of the decades dif-

ers significantly in terms of bone Mn in black females. The overallrend towards higher bone Mn in the 1990s could be due to themall sample size relative to other decades. The presence of a sin-

No significant differences were seen between individuals admit-ed to Pretoria, Johannesburg or rural hospitals. Nor were there any

able 4one Mn concentration in �g g−1 and decade of death by ancestry and sex.

Decade 1960–1969 1970–1979

N Median (SD) Range N Median (SD) Range

Black males 41 0.25 (0.24) 0.11–1.0 48 0.31 (0.32) 0.05–1.55White males 2 0.24 (0.10) 0.17–0.307 14 0.25 (0.29) 0.12–1.02Black females 23 0.29 (0.15) 0.13–0.64 20 0.42 (0.38) 0.17–1.49

0.32 0.558 0.05 4.380.25 0.068 0.09 1.680.31 0.308 0.11 1.49

significant differences in bone Mn concentration by age at death.Bone Mn was compared to other bone element concentrations. Nocorrelation was found between bone Mn and bone Pb, nor with As,Ni, Zn, or Mg. Bone Mn was significantly correlated with V (Spear-man’s r = 0.632, p < 0.0001) as well as with Cd (Spearman’s r = 0.589,p < 0.0001) and Cu (Spearman’s r = 0.553, p < 0.0001). Bone Mn wasalso correlated with bone Fe (Spearman’s r = 0.613, p < 0.0001) butonly in white South African males.

4. Discussion

The lack of significant difference in mean bone manganese, aswell as the low concentration relative to other countries suggestsa common environmental source of manganese exposure affect-ing all individuals. In these remains, in which all individuals livedand died prior to the use of MMT, bone manganese concentra-tion does not differ significantly across the sampled individuals nordoes it differ across time or place. Moreover, bone manganese con-centration in the sampled remains is comparable to manganeseconcentrations measured in non-occupationally exposed popula-tions in Spain, New Zealand or Korea which range from 0.006 to0.36 �g g−1 (Benes et al., 2000; Casey et al., 1982; Llobet et al., 1998;Yoo et al., 2002). Pejovic-Milic et al. (2009) have examined bonemanganese as an indicator of occupational exposure in Canada. Inthat study bone manganese in occupationally exposed individualsranged from 3.8 to 9.1 �g g−1 and in non-exposed individuals therange was 0.2–3.0 �g g−1. In our study, only one individual has abone manganese concentration above 4 �g g−1, a black male. Out-side of that individual, no other group has any one individual witha bone manganese concentration above 2 �g g−1. The median bonemanganese concentration of approximately 0.3 �g g−1 lies just atthe higher end of the values for these countries and could be con-sidered low to moderate exposure, given that it is above what isexpected for non-occupationally exposed individuals and far belowwhat is expected for occupationally exposed individuals (Pejovic-Milic et al., 2009). Moreover, the distribution is skewed right, andthe median is lower than the mean of 0.44 �g g−1. These values arecommensurate with bone manganese concentrations reported forRussia (0.35 �g g−1) or New Zealand (Casey et al., 1982; Zaichicket al., 2011). Notably, Canada and Russia permit the use of MMT ingasoline, though Canada largely discontinued the practice in 2006(Joly et al., 2011; Zayed, 2001).

These results are commensurate with the environmental data,which indicate that during the period from 1960 to 1998, man-ganese, although present in the atmosphere, was low relative to

1980–1989 1990–1998

N Median (SD) Range N Median (SD) Range

36 0.38 (0.67) 0.13–3.05 3 0.42 (0.38) 0.34–1.04 12 0.24 (0.26) 0.09–0.97 8 0.45 (0.64) 0.15–1.68

5 0.16 (0.17) 0.11–0.53 1 1.24

6 C.A. Hess et al. / International Journal of Paleopathology 8 (2015) 1–9

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cross the population. This is further supported by the relative sta-ility of manganese across time and space in the sampled remains.

It is impossible, as with most skeletal collections, to determinehe complete residential history of the individuals from these col-ections. Admitting hospital is used here as a proxy for determiningeographic residence. This may result in imperfect geographic, butot necessarily demographic (e.g. race and sex) results. It is possiblehat some of the black South Africans were circular migrants – indi-iduals whose legal residence was located in one of the apartheidomelands. These individuals often worked in the urban areas inining and industry for predetermined periods of time and were

hen expected to return to their homeland (Byerlee, 1974). How-ver there is also evidence that rural to urban circular migrantsended to return to their homeland upon becoming ill and were

ore likely to die in their homeland (Clark et al., 2007). This meanshat these individuals may have spent time outside of the urbanrea and had different exposure to manganese.

It remains unclear however, why bone manganese in whiteales who died between 1990 and 1998 varies substantially

ompared to other decades. Within the limited environmentalonitoring data, there does not appear to be a trend towards

ncreasing manganese in the urban environment, and the periodrecedes the introduction of MMT in the petrol supply. It coulde that this variability is simply a result of the small sample sizeor individuals who died during this decade. However, four of theight white males who died in the 1990s have bone manganese

clear trend. Without knowing the occupational history of these

ent-day Gauteng.

individuals it is difficult to speculate as to why this dichotomyoccurs in individuals who died during this decade. No othersignificant trends were apparent in this sub-group with regards tobone manganese and city of residence or age at death. We surmisethat the most likely explanation for this trend is sampling bias,a limitation of bioarchaeological investigations and the use ofskeletal collections in epidemiological studies.

Overall, we found no significant differences in bone Mn by ageor sex. The relationship between bone Mn, age and sex differs inthe literature. Zaichick et al. (2011) did report decreasing bone Mnwith age and higher bone Mn in women. Recent measurements ofbone Mn in the femoral head of hip-replacement patients in Polandfound no significant variation in bone Mn by age or sex (Budiset al., 2014). Both Zaichick et al. (2011) and Budis et al. (2014)report positive correlations between bone Mn and Fe and giventhe metabolic pathways of each element we would have expectedto find a similar relationship. Furthermore, given ferromanganesesmelting as a potential environmental source, it is unexpected thatbone Fe and bone Mn do not correlate in all individuals. Notably,in the sampled remains, white South African males showed signif-icantly lower bone Fe than black South Africans regardless of sex,which may likely be affecting these results. The reasons behindthis are unclear. Both Zaichick et al. (2011) and Budis et al. (2014)report positive correlations between bone Mn and Fe. It must bestated, however that studies of bone Fe are not widely reported inthe literature and the reliability of bone Fe measurements is not

The significant correlations between bone Mn, Cd and V areinteresting, though without further investigation, such as blood

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iomonitoring in a modern population, it is difficult to be cer-ain as to the cause. The three elements are constituents of Southfrican coal and fly ash from coal-fired power plants (Ayanda et al.,012; Kalenga et al., 2011). One possibility is that these elementsay be correlated if the source of Mn exposure in our sampled

emains is coal, which can release particulate matter into the atmo-phere via combustion or contaminate water via acid mine (AMD)rainage near coal mines (McCarthy, 2011; Moyo et al., 2011). High-eld coal in particular is highly enriched in Mn compared to otherouth African coals and compared to the global average for Mnn coal (Wagner and Hlatshwayo, 2005). In addition, low incomerban households, particularly those located within the townshipsnd in informal settlements also burn coal for cooking and heat-ng. Approximately 20% of households in Soweto and in Alexandriaownships burn coal in this way (Kimemia and Annegarn, 2011).

.1. Manganese exposure in the future

Due to the paucity of manganese exposure data in urban Southfricans, these results become valuable, particularly in light of theeplacement of lead with MMT in gasoline. Studies of lead expo-ure on adult males in the same skeletal remains yielded a clearichotomy in bone lead concentration between black South Africanales and white South African males that is likely linked to socio-

conomic and residential segregation and exposure to traffic (Hesst al., 2013). In this study white South African males showed signif-cantly higher bone lead concentration than did black South African

ales, owing largely to the fact that the latter lived in residentialreas outside of the highly congested central business district. Inhe present study of manganese, no such dichotomy exists betweenither black and white South Africans, or urban versus suburbanesidents indicating that exposure to automotive pollution is likelyot the main route of exposure for manganese prior to 2000. Inddition, there is no significant correlation between bone man-anese and bone lead in the sampled remains, which would bexpected if there was a common source for both elements. How-ver, with little change in urban residential patterns in Gauteng inhe post-apartheid era (Christopher, 2001), this is likely to changes exposure to traffic-related manganese affects the population.n addition to an increase in manganese exposure, we hypothe-ize that the pattern of exposure will mirror that of lead exposure,amely that white South Africans living in the urban core will bear areater burden of exposure to manganese through more significantxposure to traffic pollution. Although highly decentralized, massransportation in urban Gauteng, particularly Johannesburg, is stillentred around the congested central business district, resultingn greater exposure to vehicular pollution in this area (Czegledy,004).

It is unclear to what extent this expected spatial pattern in man-anese exposure is actually realized in the current population, asittle research into adult exposure to manganese has been carriedut in Johannesburg or Pretoria. What research has been carriedut has focused on blood manganese monitoring which can onlye compared to bone manganese data insofar as it highlights broadegional trends in exposure. Röllin et al. (2009) found that bloodanganese and cord blood manganese levels in women and infants

rom urban Gauteng were substantially lower than those in womennd infants from any other region, including mining and indus-rial areas. Notably, this does not follow the same trend as leadhich shows a clear urban/rural, high/low dichotomy in regards to

lood lead concentration, though this may change over time withumulative exposure (Grobler et al., 1986; Monna et al., 2006).

The results of this research demonstrate that should manganesexposure shift towards a similar exposure route to that of lead in theeriod prior to 2006 some predictable patterns may emerge. Mostotably perhaps may be the appearance of manganese hotspots

of Paleopathology 8 (2015) 1–9 7

across the urban landscape. These are likely to emerge alongtransportation corridors in and around the urban core and affectroad users and residential areas adjacent to major roadways moresubstantially than suburban residents. Demographically these resi-dents are more likely to be white residents of the urban core, orblack South Africans working in domestic settings within the urbancore or within the central business district. Most critically, man-ganese emitted from crustal (soil) sources such as ferromanganesesmelting and mining tend to be found in more coarse particulatematter (PM10) and found in the environment as inorganic man-ganese or manganese oxides (Post, 1999) and may not be as widelyas manganese found in fine particulate matter (PM2.5). Manganesefrom tail pipe emissions and other combustion activities is gen-erally found in fine PM and as manganese phosphate or sulfatewhich may result in greater neurotoxicity in humans than inorganicmanganese or manganese oxide exposure from ferromanganesesmelting (Davis et al., 1988; Dorman et al., 2006; Normandin et al.,2004).

Our data demonstrate that the urban population of Gauteng wasalready exposed to levels of manganese commensurate with thosein MMT-exposed populations such as Canada, though the form ofmanganese was likely different (Pejovic-Milic et al., 2009). Shouldmanganese exposure patterns follow the same traffic-related pat-tern as lead (and there is little reason to believe it will not), it ispossible that white South Africans and those who live or work nearthe urban core will face increased exposure to manganese phos-phate and manganese sulfate. This means for at least part of thepopulation, the degree of manganese exposure and the potentialneurotoxic effects of such may increase with increasing use of MMTin South Africa.

5. Conclusion

This research highlights the contemporaneous distribution ofmanganese exposure within an urban South African sample. Theresults show no demographic variation in exposure to manganeseand that overall exposure to manganese in the sampled remainswas low to moderate. There are however, limitations to the datapresented here. Firstly, bone is only beginning to be used as a matrixfor biomonitoring manganese in humans, despite recent researchdemonstrating the utility of in vivo neutron activation analysis asa non-invasive measurement of manganese in bone (Aslam et al.,2008; Pejovic-Milic et al., 2009). As yet, there is limited bone man-ganese data from other regions with which to compare the bonemanganese results presented here. In addition, there is no estab-lished bone manganese threshold by which clinical or subclinicaleffects of manganese is expected to appear, making it difficult tospeculate as to the health consequences that may have occurred as aresult of manganese exposure in urban South Africans. Nonetheless,these results do yield critical information regarding trends in man-ganese exposure in the sampled remains. Despite strict residentialsegregation, manganese exposure may have remained relativelyuniform across the population, a trend which is likely to change inthe future.

The widespread use of MMT as a lead replacement however,is troubling. The neurotoxic effects of manganese are clear, par-ticularly as they relate to neurological disability. Whereas theindividuals studied in this project had uniform and relatively low(compared to other countries) exposure to manganese, this willmost certainly change. Increased manganese exposure is alreadybeing reported in urban South African school children (Batterman

8 urnal

bhaLnhmlep

attUCCTPSC

lack African population, who are now free to live in neighbour-oods once strictly off limits to them, yet there is evidence thatpartheid residential patterns persist and are changing very slowly.iving conditions among new urban settlers have not changed sig-ificantly and hundreds of thousands of informal urban householdsave arisen, often near transport networks and potential employ-ent opportunities. These individuals may be exposed to similar

evels of manganese as their affluent white compatriots. Whilst theffects of manganese exposure are not as acute as those of lead, theotential for disability among the affected may be greater.

cknowledgements

The authors would like to thank Marius Loots and Ericka L’Abbet the University of Pretoria for their generous assistance and accesso the Pretoria Bone Collection. In addition, the authors would likeo thank the curators of the Dart Bone Collection at Witwatersrandniversity for access to the Student Bone Collection. Dr. Matthewooper at the University of Southampton National Oceanographyentre and Dr. Rebecca Bennett are also recognized for assistance.he research was funded in part, by the University of Bournemouthost Graduate Global Exchange Fund, the Bournemouth Universitychool of Applied Sciences Hilary Williams Fund, and the Britishouncil Overseas Student Research Award Scheme.

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