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Biol Trace Elem Res (2017) 175:237–243

DOI 10.1007/s12011-016-0745-9

Mercury Human Exposure in Populations Living


Around Lake Tana (Ethiopia)
G. Habiba 1 & G. Abebe 2 & Andrea G. Bravo 3 & D. Ermias 4 & Ǻ. Staffan 5 & K. Bishop 5

Received: 19 January 2016 / Accepted: 16 May 2016 / Published online: 9 June 2016
# Springer Science+Business Media New York 2016

Abstract A survey carried out in Lake Tana in 2015 found lightening soap on a daily basis had 2.5 times greater mercury
that Hg levels in some fish species exceeded internationally in scalp hair than non-users. Despite the different sources of
accepted safe levels for fish consumption. The current study mercury exposure mentioned above, the mercury concentra-
assesses human exposure to Hg through fish consumption tions of the scalp hair of participants of this study were below
around the Lake Tana. Of particular interest was that a dietary levels deemed to pose a threat to health.
intake of fishes is currently a health risk for Bihar Dar resi-
dents and anglers. Hair samples were collected from three Keywords Bihar Dar . Fish . Hair . Mercury . Occupation .
different groups: anglers, college students and teachers, and Residents
daily laborers. A questionary includes gender, age, weight,
activity. Frequency of fish consumption and origin of the eaten
fish were completed by each participant. Mercury concentra-
tions in hair were significantly higher (P value <0.05) for Abbreviations
anglers (mean ± standard deviation 0.120 ± 0.199 μg/g) than ANOVA analysis of variance statistics
college students (mean ± standard deviation 0.018 BoD burden of disease
± 0.039 μg/g) or daily workers (mean ± standard deviation EPA Environmental Protection Authority
16 ± 9.5 ng/g). Anglers consumed fish more often than daily FAO Food and Agriculture Organization
workers and college group. Moreover, there was also a strong Hg Mercury
correlation (P value <0.05) between the logarithms of total IPCS International Program on Chemical Safety
mercury and age associated with mercury concentration in ND not detected
scalp hair. Mercury concentrations in the hair of men were NRC National Research Council (Washington, DC)
on average twice the value of the women. Also, users of skin SMEC Snowy Mountains Engineering Corporation
UNDP United Nations Development Program
UNEP United Nations Environment Programme
* G. Habiba DTIE Division of Technology, Industry, and
habibag2@gmail.com
Economics
WHO World Health Organization
1
Ethiopian Institute of Water Resources, Addis Ababa University,
Addis Ababa, Ethiopia
2
Department of Zoological Sciences, Addis Ababa University, Addis Introduction
Ababa, Ethiopia
3
Department of Ecology and Genetics, Limnology and Science for According to the Environmental Protection Authority of
Life Laboratory, Uppsala University, SE-75236 Uppsala, Sweden Ethiopia [10] report, Ethiopia has an estimated mercury (Hg)
4
Hawassa University, Addis Ababa, Ethiopia production of 40,600 kg/year. In addition to dental amalgam
5
Department of Aquatic Sciences and Assessment, Swedish fillings (“silver” fillings), laboratory chemicals and other lab-
University of Agricultural Sciences, Uppsala, Sweden oratory and medical equipment containing Hg are the main
238 Habiba et al.

sources for water ecosystems. One of organic form methyl-Hg In Ethiopia as in many other African countries, the connec-
(MeHg) is of particular concern because it bioaccumulates and tion between dietary intake of fish and human exposure to Hg
biomagnifies in fish to levels that are many thousands of times accumulation has not been assessed; it has been however
greater than levels in the surrounding water [33]. Indeed, the shown that hair Hg concentration exceeded 50 μg/g in gold
general population is primarily exposed to MeHg through fish miners, anglers, and their families on Lake Victoria [18].
and seafood (seafood includes shellfish and marine mammals, Bihar Dar, the capital of Amhara Region, is on the southern
such as whales) consumption [37]. The toxic MeHg can dam- shore of Lake Tana where the Abay (Blue Nile) river flows
age the central nervous system [21] in severely exposed adults out. The current study aims to investigate the exposure of
[4, 15] and children [4]. For example, one fourth of house- Bihar Dar residents via fish consumption to Hg, with special
holds from Zieway islands developed a mental illness due to emphasis in anglers. Furthermore, this study also addresses
high consumption of MeHg-contaminated fish [30]. the effect of the use of skin lightening products that may
Consumption of Hg-contaminated fish could cause abdominal contain Hg, in the form of inorganic Hg salts on Hg concen-
and lower back pain, progressive weakness, paresthesias, and trations in scalp hair. Indeed, although such products are ille-
fatigue. Other researchers described that Hg-contaminated gal in many countries, they are commonly used in certain
fish causes weight loss [22], fingers curled, losing memory, African and Asian countries [36].
permanent nervous system damage, skin rash, neurological
symptoms such as dizziness or memory loss, generally a clin-
ical picture of Minamata disease seizure, hair falling, loss of Methods
hearing, and inability to concentrate [15]. It can also induce an
increase of cholesterol as a risk factor for the myocardial Study Area
infarction and coronary/cardiovascular disease [19]. Even
prenatal exposure to MeHg caused increasing of diastolic Sampling took place between December 2014 and January
and systolic blood pressures in boys at the age of 7 in the 2015, Bihar Dar city. Bihar Dar, the capital of Amhara
children from the Faroe Islands [31] and increased diastol- Region, is on the southern shore of Lake Tana where the
ic blood pressure at age 15 years in Seychelles [27]. Abay (Blue Nile) river flows out (Fig. 1). The city is located
Moreover, a study on fish-eating Amazonian communities approximately 578 km north-northwest of Addis Ababa, hav-
indicated that there are inverse relations between Hg ac- ing a latitude and longitude of 11° 36′ 0″ N and 37° 23′ 0″ E
cumulation on biomarkers and oxidative stress [16] and and an elevation of about 1800 m above sea level. In 2007, the
lower increase in blood pressure [8]. Bihar Dar Special Zone had a total population of 221,991 of
In Ethiopia, with respect to the increase of population, the that 81.1 % were urban inhabitants, with the rest of the pop-
exploitation of the food resource existing in the rivers and ulation living at rural kebeles around Bihar Dar. In the town of
lakes has received special attention. Of the total annual fish Bihar Dar itself, there are 155,428 inhabitants; the rest of
potential production of lakes, Lake Tana could contribute urban population is living at Meshenti, Tis Abay, and Zege
more than half of the estimate as it is the largest freshwater towns which are part of the Bahir Dar Special Zone [6]. At
reservoir of Ethiopia [24]. least, another 15,000 people are reported to live on the islands
Investigation on some Ethiopian lakes indicated that some of Lake Tana [29].
fish species contain high Hg concentrations. For example,
piscivorous big Barbs (Labeobarbus intermedius) in Lake Study Subjects
Hawassa has exceeded the marketing limit of the European
Union 0.5 mg/kg [7]. It has been reported that Hg concentra- Fifty-three hair samples were collected from volunteers of the
tions are significantly higher in L. intermedius than in Clarias Bihar Dar city. Those volunteers selected were from colleges
gariepinus and Oreochromis niloticus in Lake Hawassa [9] (students and teachers) (females = 7 and males = 17) with the
and Koka [9, 12]. However, Barbus intermedius seemed to age range 17–49, anglers and their families (females = 8 and
have higher THg concentrations than O. niloticus only in Lake males = 15) age range between 9 and 45, and participants with
Ziway [12]. In particular, in Lake Tana, THg concentrations in other occupation (males = 5) with the age range of 18–25,
fish muscle indicated that more than half of Labeobarbus around Lake Tana.
megastoma, 33.3 % of L. intermedius, and 31.2 % of
C. garipinus exceeded the recommended level of 0.3 μg/g of Hair Sample Collection and Analysis
Hg [17], which designed to protect at-risk groups [37]. Even 71
and 27 % of L. megastoma in March and October, 25 % Determination of Hg in hair and blood allows exposure to be
C. garipinus, and 22 % of L. intermedius in March 2014 quantified and linked to possible health effects. It also permits
exceeded the recommended [38] of 0.5 μg/g, which is the mar- estimates of the burden of disease (BoD). WHO is applying its
keting limit for Hg in fish [17]. BoD framework approach to better quantify the health
Mercury Human Exposure in Populations Living Around Lake Tana 239

Fig. 1 Bahir Dar city map

impacts [35] when the populations are not exposed to elemen- Hair Hg analysis was done at the Department of Aquatic
tal Hg. Hair samples were collected as described in [23]. Sciences and Assessment Laboratory at the Swedish
Approximately 100 strands of hair (~50 mg) were gathered University of Agricultural Sciences. Determination of total
and cut closer to the occipital region of the scalp (approxi- Hg carried out using EPA method (7473) with PerkinElmer
mately the diameter of a pencil eraser). Samples tagged and SMS 100 Hydra c. The SMS 100 uses a decomposition fur-
placed in plastic bags. nace to release Hg vapor instead of the chemical reduction
Those who were willing to give hair samples were also step used in traditional liquid-based analyzers. This instru-
asked to fill the questionnaire. They were informed about ment works using thermal decomposition and amalgamation
the confidentiality of the signed agreement before they an- coupled with atomic absorption [25]. Standard samples for
swered the questionnaire. This questionnaire was adopted calibration of hair (IAEA-085/IAEA-086) (IAEAf) have been
and modified from [33] guideline. The questionnaire includes used to control the digestion and analytical readings. The ac-
information on (1) age, (2) gender, (3) occupation, (4) fre- cepted precision level of the standard samples for 10 tripli-
quency of fish and servings, (5) fish species often served, (6) cates was higher than 97 %. Hair samples were not cleaned
presence of hair coloring, (7) health problems, and others. before analysis. Three replicates of each hair sample have
Amhara National, Regional State Health Bureau, and been analyzed, and the mean value was recorded with a stan-
Ethiopian National Research Ethics Review Committee ethi- dard deviation of (0.001 μg/g). About 0.5 mg of hair sample
cally reviewed this study. We assigned three groups identified was put on a sample boat. Sample boat was then inserted to the
under occupation: group 1, anglers and their families— SMS 100 Hg analyzer. Sample dried with 300C0 for 45 s then
they are dependent on fishing from Lake Tana in addition decomposed with 700C0 for 150 s in an oxygen-rich furnace
to their farming work; group 2, college students and to release all the decomposition products, including Hg. These
teachers—especially students who do not live on a campus. products then carried in a stream of oxygen to a catalytic
In addition, students are employed in private or governmental section of the furnace heated with 600C0 for 60s. Any halo-
organizations and they are self-sponsored; and group 3, other— gens or oxides of nitrogen and sulfur in the sample trapped on
illiterate and daily workers (horse riders around Lake Tana). the catalyst. The remaining vapor then carried to an
240 Habiba et al.

amalgamation cell that selectively traps Hg by gold trap tem- anglers, and six for the students and lecturer group drank
perature of 600–700 °C for 30 s. After the system was flushed alcohol once per week, and from the fishermen’s group, only
with a flow of 300 ml/min oxygen to remove any remain- two respondents drank alcohol once per day. No one of the
ing gasses or decomposition products, the amalgamation participants had a diagnosis of a disease consequence of THg
cell was rapidly heated, releasing Hg vapor. Flowing ox- exposure.
ygen carries the Hg vapor through an absorbance cell
positioned in the light path of a single wavelength atomic Occupation
absorption spectrophotometer. Absorbance was measured
at the 253.7 nm wavelength as a function of the Hg. Hair THg accumulation varied between the study groups
Samples (n = 20) sent to IVL Swedish Environmental (Fig. 2). Analysis of variance carried out with the normalized
Research Institute to verify the results of Hg. ln(THg) result indicates that THg was significantly (P < 0.05,
F = 6.15) higher on anglers than students and lecturer groups.
Statistical Analysis Angler groups had a median of 0.011 μg/g which was lower
THg as compared to the participants with other occupation
Distributional properties of the data and transformations re- with a median of 0.018 μg/g and higher than students and
quired to meet the assumptions of normality were checked lecturer group with a median of 0.006 μg/g (Table 1).
prior to the analysis of the data. Accordingly, THg and age
were log transformed. Differences in ln(THg) concentrations Fish Consumption
in scalp hair between groups were tested by ANOVA and
Tukey post hoc tests. Data analyses have been carried out with The frequency of fish meals/week varies between 0 and 7. It is
SPSS software (version 16.0), and statistical significance (P noteworthy to highlight the low fish consumption of volun-
value) was set at (0.05). teers, as 75 % of the participants consumed fish only once a
week. Analysis of variance results of hair THg have a positive
significant relation (P < 0.05) with fish-feeding habits of
Results whole respondents. Four respondents eat fish every day, and
63 % of angler group consumed fish once a week. Out of all
Fifty-three scalp hair samples were collected from Bahir Dar participants with other occupation and students and lecturer
residents and were analyzed for THg. THg concentrations in group, 60 and 30 %, respectively, of them had fish meal once a
scalp hair of seven individuals were below the detection limit, month (Fig. 3). This is significantly (P < 0.05) higher frequen-
and the highest concentration reported was 0.645 μg/g (mean cy of fish meal/week (mean ± SD 2.1 ± 2.7 fish meal/week,
± SD 0.069 ± 0.147 μg/g, median = 0.009 μg/g) (Table 1). P < 0.01, F = 13.08) than for the other groups with an average
Skewness and kurtosis of THg concentration distribution in- of fish meal/week followed by students and lecturer group and
dicate that most of the individuals presented low THg concen- participants with other occupation. But, hair THg did not
trations in scalp hair. Indeed, 25 % of the volunteers contained show significant variation between anglers who had fish meal
less than 0.005 μg/g and 75 % less than 0.029 μg/g THg in once daily, once per week, and does not eat fish at all. Also,
scalp hair. there is no significant variation among groups of respondents
From the questionnaire, we found a few anglers (n = 6) that who had fishmeal once per week, once in a month, and who
routinely handles gasoline or kerosene. From the participants, has no fishmeal at all for students and lecturer groups.
there were no indications of exposure to inorganic Hg.
Participants with other occupation had higher average weight Age and Hair THg
than anglers and students and lecturer groups (61.2, 57.6, and
53 kg, respectively). Out of all participants, only two of them ANOVA test result indicated that THg (P < 0.05, R2 = 0.3)
smoke cigarettes. Two participants with other occupation, four increases as age year of angler group increase. The result of

Table 1 Mean ± SD hair THg values for three respondent groups

Group Gender THg in scalp hair (μg/g) Age (range) Daily soap users Fish consumers

M F Range Mean ± SD Median Years % Users (%), serving

Anglers and families 15 8 ND–0.64 0.12 ± 0.19 0.011 9–45 34.7 % 63, 1/week
Students and teachers 17 7 ND–0.2 0.017 ± 0.039 0.006 17–49 52 % 30, 1/month
Other 5 0.005–0.028 0.016 ± 0.009 0.018 18–25 40 % 60, 1/month
Mercury Human Exposure in Populations Living Around Lake Tana 241

and 0.031 ± 0.06 μg/g, n = 16, respectively) (Fig. 2). In addi-


tion, the median value of THg for males (0.007) is higher than
females (0.005). But, the THg variation was not significant
among male and female groups. On average, THg in scalp hair
was 2.14 times higher for male than females in angler group.
Similarly, on students and lecturer group, males had high av-
erage hair THg (mean ± SD 0.012 ± 0.014 μg/g) than females
(mean ± SD 0.005 ± 0.02 μg/g).

Cosmetics, Skin Lightening Soaps, Hair Dye,


and Treatments

More than half of the participants (54 %) use skin lightening


soaps once a day, and 18.9 % of them use creams. Despite this,
the difference was not significant between soap users and non-
Fig. 2 Box plots of total mercury (THg) concentrations in scalp hair of
users; the individuals that use soaps daily accumulate 2.5
individuals grouped according to their occupation: (i) anglers, (ii) times higher THg in hair than non-users. The result of this
students and teachers, and (iii) other. THg concentration in hairs of study is consistent with [20] and [18]. Two female and two
screened women ( f ) is presented in gray box plot and in men (m) in males dye their hair once per month. One male and one female
white box plots
participant use hair treatment once per year.

this study is consistent with other studies of [23, 26].


However, THg does not show a significant correlation
(P < 0.05, R2 = 0.06) with the age of whole sample respon- Discussion
dents and the two groups other than anglers.
The hair THg levels were lower than the recommended
level of EPA [11] 1 μg/g risk level in all participants
Gender (Fig. 2), without significant differences between male
and females. As compared to other African country stud-
Analysis of THg was done in hair samples of 8 female and 15 ies in Botswana (mean ± SD 0.22 ± 0.21 μg/g) [3] (ranges
male anglers, 7 females and 17 males of students and lecturer between 48.2 and 953 μg/g; mean value > 2 μg/g, respective-
group, and 5 males of participants with other occupation ly), Tanzania [18, 20] (ranged from <0.1 to 54.8 μg/g), and
(Table 1). This study discovered that males had high average South Africa [34], this study participant had very low THg in
hair THg than females (mean ± SD 0.07 ± 0.166 μg/g, n = 37 hair. In addition, our study participants had lower hair Hg than

Fig. 3 Box plots of total mercury


(THg) concentrations in scalp hair
of individuals grouped according
to their fish consumption
242 Habiba et al.

that of studies in Romania (median 1.1 μg/g) [5], Indonesia sampled in March had Hg above the recommended levels,
(mean ranging between 13 and 17 μg/g) [4], and USA (mean indicating that this species of fish might have a risk of Hg
value ranging between 0.2 and 0.38 μg/g) [23]. Some of the contamination for human health especially in March. In
studies mentioned [4, 5, 18, 34] were carried out close to October except for one species, L. megastoma, the species
mining areas or chlor-alkali plants both known to be important sampled in Lake Tana fishing study all had lower than the
sources of Hg for the environment. However, to the best of our level of 0.5 μg/g, which is recommended by WHO/IPCS
knowledge, there are no such sources of Hg around Lake Tana [38] for marketing limit of Hg in fish.
or upstream tributaries of Nile River. Despite that high THg Nevertheless, the angler group had higher mean hair THg
concentrations have been reported on THg survey in fish from compared to participants with other occupation and students
Lake Tana, it is important to highlight the low Hg exposure of and lecturer group (Fig. 2), consistent with another study of
volunteers. Most of the studies have associated high exposure Bravo et al. [5], likely because anglers consume fish more
to Hg with high fish consumption [1, 3, 5]. However, popula- often. In addition to this, 15 participants from two groups
tions living around Lake Tana seem to consume fish rarely (daily worker and students and lecturer group) do not eat fish
(Fig. 3). This is consistent with the low fish consumption and and they had less than 25 μg/g of THg in hair. This is because
low protein intake by fish consumption reported in the year- fish is very expensive, and they cannot afford to buy it.
book of Fishery and Aquaculture of FAO [13] for Ethiopia. Similarly, Gordon et al. [14] has reported that fish is a luxury
We thus conclude that low exposure to Hg by the participants food consumed by higher income groups because its price is
is mainly due to the low fish consumption. A similar study by rising. However, the median (THg) for participants of group 3
Bełdowska and Falkowska [2] had also resulted in a sim- (other) was higher (0.018 μg/g) than the college group
ilar conclusion with this study. The levels of THg in hair (0.06 μg/g); this might be because out of group 3 participants,
in the anglers and their families were similar to the an- more than half percentage (60 %) of them had one fish
glers in Botswana with similar but slightly higher fish meal/month than the college group (30 %), indicating that
consumption by fishermen in Arbamench, Hawassa, and group 3 participants work on horse riding for transporting
Zieway (on average, once and twice a day on some days) wood and papyrus grass from the port of Lake Tana to Bahir
[30] and the Okavango River (mean ± SD 3.2 ± 2.2 Dar city. Therefore, they have access to eat fish better than the
fish/week) in Botswana [3]. college group. Although, it is true that all respondents eat food
There are other possible factors explaining the low concen- produced around Bahir Dar.
tration of THg in scalp hair of our participants. One of those In this study, THg concentrations in hair were slightly
could be seasonal variability of Hg accumulation in fish of higher in males compared to females (Fig. 2), although the
Lake Tana. According to the Lake Tana fish THg study [17], difference was not significant. This is consistent with other
THg was high in March 2014 and it was low in October 2014. studies of [28] and [26].
In addition, human hair samples were taken in between Although we do not have statistical evidence to conclude
November and December, which is the fast preceding about the effect of skin and hair lightening products on THg
Christmas for orthodox religion followers for 40 days between concentrations in scalp hair, we observed a higher concentra-
25 November and 9 of January [32] during this time people tion of THg in the hair of daily users. Therefore, the concen-
who are fasting do not eat fish (even this is controversial). The tration of Hg in soaps and cosmetics we are using has to be
other condition might be 50 % of respondents prefer to eat studied in the future.
O. niloticus than other species of fish. Participants of this
study have the same fish preference with those fishermen
studied by [30]. In our fish Hg survey we have carried out in Conclusion and Recommendations
parallel study [17], we found that O. niloticus has a very low
Hg concentration in March 2014 and October 2014 (mean This is the first study assessing human exposure to Hg using
± SD 0.066 ± 0.013 and 0.062 ± 0.067 μg/g, respectively, com- hair in Ethiopia. Specifically, this study assessed the effect of
pared to other sampled species of fish in Lake Tana. occupation, age, frequency of fish meal, gender, and skin
Moreover, from the three species sampled in March, lighting soap on the THg concentration of scalp hair in 53
L. megastoma, L. intermidius, and C. garipinus (>50, 33, volunteers. Generally, the concentration of Hg in Bahir Dar
and 31 %, respectively) in the Lake Tana fishing study, all resident’s hair was well below internationally accepted levels
had higher than the level of 0.3 mg/kg, which is designed to of risk of Hg exposure due to low consumption of fish. Hair
protect at-risk groups [37]. In addition to this, 70, 25, and Hg shows variation based on occupation, and the angler group
22 % (L. megastoma, L. intermidius, and C. garipinus, respec- had higher mean hair Hg compared to participants with other
tively) of March samples exceeded the recommended [38] occupation and students and lecturer group. In addition to this,
standards of 0.5 μg/g for Hg content. Therefore, males had somewhat higher hair Hg than females. Although
Labiobarbus species of fish and C. garipinus which were we did not estimate the concentration of Hg in soaps and
Mercury Human Exposure in Populations Living Around Lake Tana 243

cosmetics, it seems that daily cosmetic users presented higher 14. Gordon A, Sewmehon D, Melaku T (2007) Marketing systems for
fish from Lake Tana, Ethiopia: opportunities for improved market-
THg concentration in scalp hair. This study was carried out in
ing and livelihoods. International Livestock Research Institute,
an area without point sources of Hg. More studies should be, Nairobi, p 49
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Acknowledgments I would like to acknowledge the following
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organizations that contributed to the completion of this work:
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Bishop K Mercury concentrations in different fish species from
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J Prev Med Public Health 38:401–407
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