Arsenic Poisoning Alters the Composition of Skin Microbial Flora of Human
Tania Sultana Bonny
M. Anwar Hossain
Arsenic toxicity causes immunosuppression and skin lesions in human beings. These two factors govern the composition of normal skin microbial flora. Therefore, the aim of the investigation was to determine, if there is any alteration of skin bacterial composition in arsenicosis patients compared to control healthy population. The microbial load and composition in skin swab samples, collected from three anatomical sites of 15 arsenicosis patients and 10 healthy control populations were analyzed by using culture techniques in nutrient agar and selective media. Finally, the organisms were identified by biochemical test and/or PCR methods. The results revealed that the total microbial count was much higher in arsenicosis patients over control populations. Composition of the bacterial isolates revealed that the Gram-negative bacterial load increased significantly in arsenicosis patients compared to control populations. In contrast, a decrease of Gram-positive bacterial load in arsenicosis patients was observed. Various genera of the Gram-negative bacteria- Proteus sp., Enterobacter sp., Acinetobacter sp., Escherichia coli, Pseudomonas sp., Moraxella sp., Klebsiella sp. and Neisseria sp. were isolated from arsenicosis and control individuals. The statistical calculation of the rate of occurrence of individual Gram-negative organism associated with the arsenicosis patients over control populations revealed that E. coli and Pseudomonas sp. (|Z| = 2.16) were the most predominant candidates. Other candidates like Acinetobacter sp., Moraxella sp., Klebsiella sp. and Neisseria sp. were found in arsenicosis patients but were absent in controls. The results clearly support our hypothesis and conclude that arsenic poisoning alters composition of skin microbial flora.
to cite this article:
Anirban Jyoti, Tania Sultana Bonny and M. Anwar Hossain, 2011. Arsenic Poisoning Alters the Composition of Skin Microbial Flora of Human. Research Journal of Microbiology, 6: 524-533.
Received: March 27, 2011;
Accepted: May 05, 2011;
Published: June 23, 2011
Inorganic Arsenic (As) is a natural element of earths crust, species
of which are found throughout the environment. More than 100 million people
worldwide have been estimated to be chronically exposed to arsenic through drinking
water containing high levels of arsenic and food-chain arsenic (Chowdhury
et al., 2000; Alaerts et al., 2001;
Islam et al., 2004a, b;
Chowdhury et al., 2006). Exploitation of groundwater
from wells has resulted in mobilizing the arsenic and led to mass poisoning
in the arsenic affected region which is defined by the generic term arsenicosis
(Rahman et al., 2001) and the process may take
between 5 and 15 years to reveal clinical manifestations of arsenicosis (British
Geological Survey, 1998; Mazumder et al., 1998b).
ATSDR (1997) has ranked arsenic as the highest in the
priority on a list of top 20 hazardous substances. Almost every physiological
system in the human is adversely affected by prolonged exposure to high doses
of arsenic (Gorby, 1994; Morton and
Dunnette, 1994). According to epidemiologic studies and clinical observations,
arsenic is associated with increased risk for certain types of human cancers
including epidermoid carcinomas of skin, lung cancers and possibly liver cancers
(Chen et al., 1992; Yu et
al., 2006; Chen et al., 2010).
There is strong evidence from epidemiological studies of an association between
chronic exposure to inorganic arsenic and hyperpigmentation, hyperkeratosis
and neoplasia in the skin as well as other diseases (Vega
et al., 2001; Dastgiri et al., 2010).
Hyperpigmentation and keratoses caused by arsenic are quite distinctive. Hyperpigmentation
is marked by raindrop-shaped discolored spot, diffuse dark brown spots, or diffuse
darkening of the skin on the limbs and trunk (Mazumder et
al., 1998b). Patchy hyperpigmentation, a pathologic hallmark of chronic
exposure, may be found anywhere on the body but occurs particularly on the eyelids,
temples, axilla, neck, nipples and groin (ATSDR, 1990).
Simple keratosis usually appears as bilateral thickening of the palms and soles
while in nodular keratosis, small protrusions appear on the palms and soles,
with or without nodules on the dorsum of the hands, feet, or the legs (Mazumder
et al., 1998a).
The trivalent inorganic form of arsenic, arsenite [As(III)] and the pentavalent
form, Arsenate [As(V)], are both contaminants of groundwater and foods but arsenite
is the more toxic of the two (Joshi et al., 2003;
Mahata et al., 2004; Spallholz
et al., 2004). Several studies have also demonstrated that arsenic
is immunotoxic (ATSDR, 1999). Arsenic toxicity has effects
on lymphocytes (Ostrosky-Wegman et al., 1991)
and interferes with the antigen-presenting function of splenic macrophages (Sikorski
et al., 1991). It is also able to alter the response of IgM and IgG
antibody-forming cells to sheep erythrocytes and the proliferative response
of lymphocytes to phytohemagglutinin (Savabieasfahani et
al., 1998; Gohar and Mohammadi, 2010).
Skin is the first line body defense of human and intact healthy skin is impermeable
to many pathogenic as well as opportunistic microorganisms (Tortora
et al., 1998). The most superficial layer of the epidermis, the stratum
corneum, is composed of flattened dead cells (corneocytes or squames) attached
to each other to form a tough horny layer analogous to a wall of bricks (corneocytes)
and mortar (lipids) and serves as the primary protective barrier (Larson,
1999). However, certain microorganisms still can grow, harbor and create
the micro-environment on skin causing the formation of normal skin microbial
flora. This flora is mostly Gram-positive in nature and behaves synergistically
with human skin and antagonistically with Gram-negative pathogens (Brooks
et al., 2001). The bacterial flora of skin consists primarily of
staphylococci, micrococci, corynebacteria and propionibacteria (Davis,
1996; Cogen et al., 2008; Willey
et al., 2008). Staphylococcus aureus is widespread in nature
and commonly found on human skin, skin glands and mucous membranes (Davis,
1996; Nagase et al., 2002). The distribution
of these skin bacteria in normal healthy individuals has been detailed previously
(Willey et al., 2008). However, traumatic injuries
produce breaks in the skin that may lead to life-threatening infectious diseases.
Persons with burns, surgical incisions, or other serious wounds are highly susceptible
to infections. Wounds expose underlying tissues to dangerous pathogens. In addition,
the reduced blood supply to the traumatized tissue often impairs the ability
of protective immune and phagocytic cells to reach the affected area (McKane,
We hypothesized that various skin lesions and consequent disruption and immunopathogenicity due to chronic ingestion of inorganic arsenic will change the composition of the human skin normal flora. The present study was therefore undertaken to investigate the composition of normal flora of skin in patients with arsenicosis and was compared with that of the healthy individuals and thereby attempt to find out any correlation of skin normal flora with arsenic poisoning.
MATERIALS AND METHODS
Subjects and clinical samples: To assess the effect of arsenic on the skin surface microbial population and composition, skin swab samples from 15 arsenicosis patients as subjects and 10 healthy individuals as control were randomly collected over a period of six months (May-October, 2006). Among these participating subjects, 12 subjects were male and 3 were female. The Subjects in this study comprised of 15 (N) individuals who were arsenicosis patients with characteristic histopathological changes in skin and had been exposed to arsenic contaminated water for at least 6-8 years (designated as Type A). Melanosis and keratosis characterized by reddish rash and pigmentation on skin and often in sever cases, skin rupture were apparent in these subjects and they had been picked from Skin and Dermatology out door unit of Bangabandhu Sheikh Mujib Medical University (BSMMU) Hospital (n = 7) as well as affected locality (Nowanagar and Nazirpur village, Sonmandi Union, Sonargon Upazila, Narayangonj, (n = 8) under the supervision of a clinical practitioner of Skin and Dermatology Unit of BSMMU. A control group comprising of healthy individuals (designated as Type B) was also included in this study. Sampling sites were carefully selected and samples were solely collected from sites where characteristic lesions were evident of arsenicosis. These sites included three anatomical sites: fore arm, finger web and upper chest.
Patients history: All patients in this study were supplied with a questionnaire. Personal information with arsenic related medical history was obtained and documented from all participants of the study which included name, sex, age and occupation, treatment taken, safety measures adopted and participants knowledge on arsenic transmission, prevention and medication.
Sampling procedure: Skin swab samples from both subjects and control group were initially taken from different skin surface sites by moistening the sterile swab into the nutrient broth containing 10% Tween 80 and skin micro flora were collected by rubbing the moist cotton swab for at least 8 times over the surfaces. Sterile screw capped test tubes containing nutrient broth with 10% Tween 80 were used to immerse and carry these swabs to the laboratory.
Quantitative and qualitative analyses: Following incubation for 4 hours in a shaker incubator (at 37°C, 120 rpm), quantitative bacterial analysis was done by 10-fold serial dilution using spread plate method on Trypticase soy agar containing 0.1% Tween 80. Cultural, morphological and biochemical characteristics of the bacterial culture were observed similarly using different selective, differential and biochemical media.
Statistical analysis: The mean bacterial population is calculated from duplicate cultures taken from right and left sides of the body from each site in each subject. Demographic variables such as gender and age were assessed. Age was categorized by decades into three groups, with the youngest one being under twenty one years and the oldest group over 50 years. Age group under 10 years is excluded from this study. To assess the significance of occurrence of isolates between the two groups of subjects by test hypothesis, following equation of hypothesis is followed:
|| Rate of significance
||Total number in a group (n1 = in arsenicosis patient group,
n2 = in healthy control group)
||Occurrence per subject in arsenicosis group, PA= a/total number
||Occurrence per subject in arsenicosis group, PB = b/total number
||(a+b) / (1/n1 +1/n2)
If |Z| >1.96, the result is assumed to be significant.
As arsenic toxicity impairs immune system and damage skin texture, it had been hypothesized that both of these factors governs skin microbial flora to change. Various types of skin lesions were found in these subjects due to drinking of arsenic polluted water for a prolonged period. Of the total 15 subjects, red rashes were found in 8 patients, pigmentation problem in 11 and skin rupture in 7. Detailed observations revealed presence of two or more of these symptoms in the patients at a time.
Total microbial load comparatively higher in arsenicosis patients: The pattern of microbial load is similar in both arsenicosis patients and control population, where the order of microbial load was: Fore arm> Finger web>Upper chest. The total microbial count was much higher in arsenicosis patients over control populations. In arsenicosis patients, the most heavily loaded microbial site was fore arm containing 7.05 log10 cfu cm-2, whereas microbial load of the upper chest and finger web were 3.55 and 5.2 log10 cfu cm-2, respectively. When compared to arsenicosis patients, microbial count was found significantly lower in the skin of control populations. The fold increase of microbial load in arsenic patients over control populations maintains the order: Finger web> Fore arm > Upper chest = 2.6>2.39>1.78 (Table 1).
|| Total bacterial count
|*Total bacterial count has been assayed in terms of log10
i.e., total bacterial count = log of (colony per plate x dilution factor/square
centimeter); cfu: colony forming unit
||Occurrence of Gram-negative and Gram-positive isolates (n
Gram-negative bacteria predominate over Gram-positive in arsenicosis patients: To verify whether there was any change of microbial composition of Gram-positive or negative microbes on the skin, we isolated a total of 159 of which 127 were isolated from 15 arsenicosis patients and that of 32 colonies from 10 control populations. Total 67 out of total 159 isolates were Gram-negative species and 92 were Gram-positive (Table 2). The fold increase of Gram-negative bacterial load on the arsenicosis patients was found 1.75 times higher over the increase of Gram-positive bacteria (Table 2).
Escherichia coli and Pseudomonas sp. predominate in arsenicosis patients: As the load of Gram-negative bacteria was found higher in arsenicosis patients over control, the frequently occurring Gram-negative microbes present in arsenicosis patients were identified. Various species and genera of the Gram-negative isolates were identified based on their culture characteristics and biochemical properties. The identified floras were Proteus sp., Enterobacter sp., Acinetobacter sp., E. coli, Pseudomonas sp., Moraxella sp., Klebsiella sp. and Neisseria sp. (Table 3).
A total of 57 Gram-negative isolates were recovered from arsenicosis patients skin, of them 20 (35.08%) were associated with red rash skin, 20 (35.08%) with pigmented skin and 17 (29.84%) with ruptured skin. The significant proportion of occurrence of the individual organism associated with the arsenicosis patients over control populations was calculated using statistical method, the test of null hypothesis (if |Z|>1.96, the results seem to bear the significant difference between two groups). The results were presented in Table 3 indicating that E. coli (|Z| = 2.16) and Pseudomonas sp. (|Z| = 2.16) were the most predominant Gram-negative bacteria in the arsenicosis patients compared to control populations.
Microbial species found on the skin surface of the arsenicosis patients
and the control: The normal skin represents a distinct ecosystem with characteristic
micro flora. The resident micro flora of human skin comprises several bacterial
genera, including staphylococci, micrococci, corynebacteria and propionibacteria
(Davis, 1996; Cogen et al.,
2008; Willey et al., 2008). Results in the
previous section clearly indicate an alteration of the composition of commensal
microflora. Therefore, we examined the composition of different Gram-positive
and negative bacteria present on arsenicosis patients skin. The results
were presented in Table 4.
|| Frequency of occurrence of Gram-negative isolates in subjects
|Arsenicosis patients were further sub-divided into three groups
depending on their lesions, rash, pigmentation or skin-rupture which can
be found in more than one participants. |Z| is the significant rate of proportion
between the two groups where |Z|>1.96 indicates that the difference between
two groups is significant
|| Presumptive types of bacteria isolated (n = 159)
|*No. of isolates occurring per group, Value in parenthesis
are percentages. -: Not present
Among all the Gram-positive staphylococcal species, 13 (10.24%) Staphylococcus
aureus and 9 (7.08%) Staphylococcus epidermidis isolates were found,
whereas these values were 4 (12.5%) and 3 (4.38%) in control group. β-haemolytic
Staphylococcus sp. isolate count was 5 (6.30%) in arsenicosis patients
but only 1 (3.13) in healthy persons. Alpha, beta and gamma streptococcal species
were also observed in both arsenicosis patients and healthy persons. Among them
a lower number of β-hemolytic Streptococcus sp. was found in arsenicosis
patients (7.87%) than healthy persons (12.5%). Beside these staphylococcal and
streptococcal species, other Gram-positive isolates were also found from the
specimens of both groups. These were Micrococcus sp., Propionibacter
sp., Bacillus sp. and Lactobacillus sp. Among Gram-negative
bacteria, Proteus sp. was found to occur in higher number among both
the groups (8.66% in arsenicosis patients and 12.50% in control). In contrast,
fewer isolates of Enterobacter sp. was found (7.87%) in arsenicosis patients
than in healthy persons (12.5%) (Table 4).
Arsenic is a metalloid and is recognized as one of the top 20 listed toxic
substances. Its occurrence in nature through drinking water has made the greatest
environmental devastation among all. The scale of this environmental disaster
is greater than any seen before; it is beyond the accidents at Bhopal, India,
in 1984 and Chernobyl, Ukraine, in 1986 (Smith et al.,
2000). Millions of people worldwide are exposed to drinking water containing
naturally occurring arsenic. In this study we have made the unique observation
that arsenicosis not only affect human by producing malignancies but also affect
their normal microbial flora of the skin.
From present study, it is evident that microbial flora of human skin varies
quantitatively and qualitatively due to chronic arsenic ingestion through drinking
well water. An increased number of bacterial loads in skin sample in arsenicosis
patients have been found as compared to the total bacterial count of skin microbial
flora of normal healthy subjects. We have also found that the total number of
Gram-negative bacteria is rationally increasing over Gram-positive ones in arsenicosis
patients. It is interesting to note that some Gram-negative species were present
only in arsenicosis patients but never in healthy subjects. Though some Gram-negative
isolates e.g., Proteus sp., Acinetobacter sp., Escherichia
coli and Pseudomonas sp. have been found from skin swab samples,
their rate of occurrence have been found significantly higher in arsenicosis
patients. The Gram-positive flora usually predominates in normal physical condition
in skin though its composition may vary with environment. The Gram-negative
bacteria we observed increasing significantly in arsenicosis patients are also
present in normal skin (Davis, 1996; Cogen
et al., 2008). However, E. coli and Pseudomonas sp.
isolated are the predominant members from the skin of arsenicosis patients.
There are reports that some of the species of these two bacteria are As-resistant
and can convert more toxic As (III) to As (V) by utilizing As-oxidase enzyme
(Chang et al., 2008; Cai
et al., 2009; Chauhan et al., 2009;
Salam et al., 2009). Present isolated E. coli
and Pseudomonas sp. from arsenicosis patients were found resistant to
both As (III) and As (V) at a concentration of more than 20 mM and showed chemotaxis
towards As (III) (data not shown) like bacterium Herminiimonas arsenicoxydans
(Muller et al., 2007). Hashem
and Abed (2002) isolated similar bacterial populations as ours from
nails and hair of women who were contaminated with As and Pb. Their results
corroborated present findings. Furthermore, poor arsenicosis patients with unhygienic
living style are prone to these As-resistance bacteria and thus lead to their
colonization. Furthermore, arsenic toxicities have the devastating immunosupperessive
effects in human and as the chronic ingestion of arsenic causes various skin
related abnormalities including malignancies (cancer), skin lesions and rupturing,
it must alter or affect the composition of normal skin flora. All present findings
strongly support this hypothesis. The apparent alteration of skin microflora
and the predominance of opportunistic and potentially pathogenic Gram-negative
species may be responsible for some of the clinical symptoms like gangrene as
one of the late stage complications in arsenicosis patients.
In conclusion, the results described here clearly demonstrated that the total bacterial load was higher in arsenicosis patients compared to healthy populations and the normal bacterial flora on skin of arsenicosis patients predominantly shifted from Gram-positive to Gram-negative bacteria. The patho-physiological mechanism of this change needs further elucidation.
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