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H I G H L I G H T S G R A P H I C A L A B S T R A C T
A R T I C L E I N F O A B S T R A C T
Keywords: Rural communities in Africa consistently lack access to safe drinking water, free from chemical contaminants and
Water filtration pathogens. One of the approaches to improve access to drinking water in these areas is point of use treatment,
Plant xylem using household water treatment devices. The objective of this work is to demonstrate the applicability of plant
Groundwater
xylem filtration, as a water treatment device for households in rural Africa. Pine xylem acted both as a physical
Africa
Safe water
filter and a cation exchanger, removing suspended contaminants and positively charged chemicals. For example,
Escherichia coli bacteria (E. coli) was completely attenuated during xylem filtration, whereas waterborne viruses
(i.e., T4) could not be removed, due to the small size of viruses. Removal of inorganic anion contaminants, i.e.,
fluoride and nitrate, was ineffective, as was the removal of negatively charged arsenate (removed by merely
40%). On the other hand, removal of six, positively charged, toxic metals was in the range of 70%–100%:
Cadmium, copper, lead, chromium, cobalt and nickel. Treatment of natural water was successful principally for
groundwaters, which contained low level of suspended material and dissolved organic matter. In this case,
filtration could produce 5 L of treated water (for xylem of 1.5 cm diameter), enough to supply the minimum daily
* Corresponding author.
E-mail address: yaalle@jce.ac.il (Y. Lester).
https://doi.org/10.1016/j.gsd.2022.100802
Received 8 January 2022; Received in revised form 12 June 2022; Accepted 26 June 2022
Available online 8 July 2022
2352-801X/© 2022 Elsevier B.V. All rights reserved.
N. Ibrahim et al. Groundwater for Sustainable Development 18 (2022) 100802
consumption required for one person for survival. In conclusion, Pine xylem can serve as an effective household
treatment device for groundwater contaminated with bacteria and toxic metals.
1. Introduction that is based on a local, available, and cheap material is likely to provide
a long-term sustainable solution. A typical example for an effective
The United Nations Sustainable Development Goals (SDGs), adopted product is the widely distributed ceramic filter: The Potters for Peace
in 2015, guide development to improve equity and health around the (PFP) filter (Lantagne 2001), which is produced in Nicaragua from
world (https://www.un.org/sustainabledevelopment). Two SDGs (the native materials and distributed to local houses by NGOs. The PFP
third and the sixth) relate directly to clean water availability. They showed to be effective in removing waterborne bacteria, but could not
emphasize the importance of access to clean water and sanitation for all, remove viruses, due to their smaller size. No other water contaminants
and the need to prevent deaths of infants and children under 5 years of were tested. In addition, filtration rate decreased markedly over time,
age. Despite these SDGs, adequate access to safe drinking water con especially in turbid waters. Filtration devices in general are an attractive
tinues to be a challenge in most developing countries, notably in rural option for household treatment, since they can make use of locally
areas of Africa and Asia (World Health Organization 2019; Rakotoma available and inexpensive porous media, they are simple and easy to use
nana et al., 2020). In sub-Saharan Africa, a quarter of the population and can potentially remove bacteria and other contaminants (Lantagne
does not have access to safe drinking water (Armah et al., 2018). 2001).
Common drinking water sources in rural Africa include shallow One of the porous material previously proposed for household water
boreholes, groundwater-wells, springs, rivers, and other local reserves filtration is plant xylem (Boutilier et al., 2014). Xylem is a porous tissue
(Armah et al., 2018). These provide water for the majority of the pop material, composed of a variety of specialized tube-like cells, responsible
ulation. In Uganda, for example, where 80% of the population live in for water conduction in plants. The diameter of these closed-end parallel
rural communities and informal settlements, access to piped, treated conduits is often too large for an effective water filtration (>10 μm).
water remains low (Nayebare et al., 2014). Treated water, supplied by However, conduits are connected to adjacent conduits via ‘‘pits’’,
the Ugandan National Water and Sewerage Corporation, is found pre covered with membranes with pores in the range of a few nanometers to
dominantly in urban areas, only available to approximately 17% of the a few hundred nanometers (depending on the species of plants), suitable
population (Nayebare et al., 2014; Zerbo et al., 2020). for attenuating many water contaminants. Employing plant xylem for
Local, unprotected water sources, in Uganda and elsewhere in Africa, household water treatment is highly advantageous, as it is a local and
are often contaminated with bacteria and other pathogenic organisms, cheap material, easily available in many rural areas. A filtration system
as a result of poor sanitation facilities (Fewtrell and Colford Jr. 2004). based on xylem involves forcing of water through the cross-section of a
Waterborne pathogens cause diarrheal diseases, which lead to the death cut plant stem. As water flows through the xylem, it crosses the pits
of more than 800,000 people globally each year (many of them children membranes, which may attenuate pathogens and other contaminants
under the age of 5, World Health Organization, 2019), and are a major (Boutilier et al., 2014; Ahmad Ansari et al., 2019).
factor in undernutrition in low- and middle-income countries (Swinburn The potential of this filtration method was demonstrated earlier by
et al., 2019). In East Africa, for example, improved water sanitation has Boutilier et al. (2014), who used pine xylem to filtrate contaminated
been associated with improved growth in young children (Rakotoma deionized water. The researchers found that the specific xylem could
nana et al., 2020). In Uganda, waterborne diseases (specifically diar effectively attenuate dead bacteria, and thus has high potential as a
rheal diseases) are the sixth leading cause of death (Center for Disease household treatment device. Still, large amounts of data are missing for
Control and Prevention, 2019). the full-scale application of this treatment method, notably: (i) filtration
In addition to microorganisms, natural water often contains different effectivity of live bacteria, which may differ from dead ones due to, for
inorganic contaminants, such as nitrate (NO−3 ), fluoride (F− ) and toxic example, the production of extracellular polysaccharide substances, (ii)
metals, originating from natural and anthropogenic sources (Yabe et al., data on filtration with xylem from different tree types, since confining
2010; Fernández-Luqueño et al., 2013; Akhtar et al., 2021; Fisher et al., the method to pine highly limits its geographical application, (iii)
2021; Owamah et al., 2021). Unlike pathogenic microorganisms, which filtration effectivity of other important water contaminants, such as
causes acute illness, exposure to inorganic contaminants through toxic metals and waterborne viruses and, most importantly, (iv) data on
drinking water mostly leads to chronic illnesses (Biney et al., 1994; Fu xylem filtration of natural waters, containing large amount of back
and Xi 2020). Analysis of drinking water in Southwestern Uganda found ground constituents such as organic matter and suspended material.
contamination with multiple metals, including lead, iron, and cadmium The hypothesis of the present study is that plant xylem, from a va
(Kasozi et al., 2019). riety of trees, can be used to remove key contaminants from natural
One of the approaches to improve access to drinking water in rural waters, providing safe drinking water for at least one person per day.
Africa is point of use treatment, using household water treatment de Subsequently, the general goal of the study was to determine the
vices (Fewtrell and Colford Jr. 2004). The main advantage of this applicability of plant xylem as a household treatment device, through
approach is its low cost, availability and the prevention of contamina (a) the analysis of the effectiveness of different xylems in removing live
tion taking place during collection, transport, and storage (Clasen and waterborne bacteria and viruses, and relevant toxic metals and ions and
Cairncross 2004; Clasen et al., 2004; Lantagne et al., 2006; Clasen (b) examine filtration of natural waters from different sources.
2015). Point-of-use approaches have gained popularity since 2003, with
the foundation of the international network to promote Household 2. Material and methods
Water Treatment and Safe Storage (HWTS), under the WHO, aiming to
promote HWTS among vulnerable populations and reduce waterborne 2.1. Materials
disease (World Health Organization 2019). Some widespread HWTS
options include on-site chlorination, filtration and solar disinfection Branches for filtration tests were taken from different trees (Table 1),
(WHO/, 2012). Their use, in conjunction with hygiene education and located on private properties in Israel. Escherichia coli (E. coli, ATCC
sanitation, is considered an intermittent solution until the infrastructure 35218), used as model bacteria, was purchased from Hy-Labs (Rehovot,
to reliably deliver safe water to the entire rural population is created. Israel), as well as the Luria–Bertani (LB) medium used to grow and
A successful implementation of a household treatment technology maintain the bacterial culture. T4 bacteriophage (ATCC 11303-B4),
largely depends on the availability and cost of materials. A technology used as a model for waterborne viruses, was a donation from the
2
N. Ibrahim et al. Groundwater for Sustainable Development 18 (2022) 100802
Pharmaceutical Engineering laboratory (Azrieli College of Engineering, near Jerusalem, receiving their water from small tributaries. All samples
Jerusalem). Sodium fluoride, sodium nitrate, cadmium chloride, copper were collected in clean 2.5 L amber glass bottles, kept in an ice box, and
sulfate, lead bromide, chromium nitrate, cobalt chloride and nickel immediately transferred to the laboratory for analysis (within 24 h).
chloride, all with 99% purity, were from Sigma Aldrich (Rehovot, Total organic carbon (TOC) was measured using a TOC analyzer
Israel). Deionized (DI) water was taken from a Direct-Q3 UV system (Acqurey TOC, Langenselbold, Germany). Fluoride (F− ) and nitrate
(Millipore). All chemicals were used as obtained. (NO−3 ) were analyzed by an ECO Ion Chromatograph (Metrohm,
Switzerland). Other water quality parameters were analyzed using
standard methods (APHA, 2005).
2.2. Filtration setup and procedure
In a typical filtration experiment, a 2-cm long section was cut from a 3. Results and discussion
branch, the bark was peeled off, and the piece was inserted into a plastic
threaded adapter reducer nipple. The nipple was tightened to a 2-L 3.1. Filtration with xylem from different types of trees
plastic pipe which served as a feed container. The xylem was sealed
with rubber bands to avoid leaks. The water solution was spiked with the Different types of trees have differently structured xylem, which may
tested contaminant and placed inside the feed container, which was affect their filtration capabilities. For example, angiosperms (flowering
sealed and pressurized using a nitrogen tank connected to its upper side plants) have relatively large and long xylem vessels (centimeters to
(at approximately 5 psi; 34.5 kPa). Filtrate was collected from the bot meters in length); compared to gymnosperms (conifers), which have
tom in glass vials. thin and short tracheid (less than 1 cm in length). Separation of con
For E. coli filtration, bacteria were first grown in 50 mL liquid LB taminants during xylem filtration is effectively done by pit membranes,
medium to optical density (OD600) of approximately 1, corresponding to connecting the parallel xylem conduits, which have pore-sizes in the
approximately 108 colony forming units per mL (CFU/mL). A pre nanometers to hundred nanometers range. Consequently, gymnosperms
determined volume from the concentrated stock was then added to the will have a larger number of pits in a 2-cm long wood, as compared to
tested water, to achieve the desired initial concentration. For T4 filtra angiosperms, and are expected to filtrate water contaminants much
tion, the bacteriophage was first propagated using E. coli as the host in more effectively (Boutilier et al., 2014).
nutrient broth (Acumedia). Following propagation, the solution was To test this hypothesis, we used several angiosperms and gymno
centrifuged (10 min, 8000 × G) and filtered through a 0.45-μm low sperms for water filtration, all abundant in Africa (Table 1) (Gessesse
protein binding filter (PES Stericup filter, Millipore), to remove cellular and Teklu 2004; Lantschner et al., 2017; Gandji et al., 2018, www.cabi.
debris. A few mL of the T4 stock were added to the water solution, to org/isc/). Experiments in this section were done using 1.5 cm diameter
achieve the initial concentration of approximately 106 plaque forming brunches, filtrating 200 mL saline solution (0.9% NaCl) spiked with
units - PFU/mL. Filtration of ions and toxic metals was done by adding E. coli bacteria at initial concentration of approximately 1000 cfu/mL.
the contaminants to tap water, and measuring their concentrations Two key parameters were tested, removal of bacteria and filtration flow
before and after filtration. rate. Surprisingly, many of the examined angiosperms removed more
than 90% of E. coli bacteria. Complete removal was achieved for Pine (a
conifer) and Populus (an angiosperm), whereas Eucalyptus and Moringa
2.3. Analytical methods had the lowest removal (7% and 13% removal, respectively). Filtration
flow rates varied between trees, from 12 mL/min for Almond to 20–25
E. coli were enumerated by the drop plate method (Chen et al., 2003). mL/min for Moringa. In general, trees with the highest filtration rates
In brief, samples were serially diluted in saline water, and 20 μL of the had lowest removal of bacteria (Eucalyptus and Moringa), indicative of
diluted sample was dropped onto mFC agar plates (in triplicates). Plates large xylem conduits with little pit membranes.
were incubated for 24 h at 37 ◦ C. The E. coli colonies were counted to Our results imply that some species of angiosperms may nevertheless
determine bacterial concentration. T4 samples were enumerated by the be suitable for water filtration. This observation is significant since an
double agar layer method (Wolf et al. 2018). Metals in the water were giosperms are much more abundant than conifers in Africa (Kalema and
quantified by Inductively Coupled Plasma Optical Emission Spectrom Hamilton 2020). Based on our results and a previous study (Boutilier
etry (ICP-OES, Spectro Genesis, Kleve, Germany). Analytical quality et al., 2014), pine tree was selected for further analysis.
control included weekly analysis of a certified reference standard (Fluka
Analytical, 90243 for ICP) and replicate analysis of samples and blanks.
Prior to analysis, samples were acidified with 2–3 drops of 70% nitric 3.2. Correlation between filtration area and volume of water filtered
acid. Each sample was analyzed three times and the results are expressed
as mean ± SD (SD: standard deviation). Relative standard deviation The maximum volume of water that can be filtered (MVF) is a crucial
(RSD) of the three results was less than 5% for all metals. Limit of parameter in designing a household filtration device, since it can limit
quantification for the tested metals was 5–10 μg/L. the system’s applicability (or the mode of application). Filtration flow
Groundwater samples were collected from two operating pumping rate is not a suitable parameter in this case, since it gradually decreases
wells (prior to disinfection), supplying drinking water to nearby com during filtration of large volumes. The MVF was calculated herein as the
munities. Surface water was taken from two different recreational ponds filtered volume of water passed through the xylem until filtration rate is
Table 1
Filtration of 200 mL saline water, spiked with E. coli bacteria, by different trees.
Tree Group E. coli conc. (cfu/ml) Removal Filtration flow (mL/min)
3
N. Ibrahim et al. Groundwater for Sustainable Development 18 (2022) 100802
decreased by 50%. Filtration in this section was done using saline water
spiked with E. coli.
Clearly, increasing filtration area increased the MVF (Fig. 1). In
general, one piece of 9.61 cm2 (equivalent to 3.5 cm in diameter) can
supply a daily water consumption of approximately 3 L, which is
considered by the WHO as the minimum required for one person for
survival (WHO 2013). In cases where higher capacity is required, a
larger piece should be applied, or the piece can be replaced during
filtration. It is noteworthy that, first, E. coli removal remained 100%
throughout filtration and, second, the average filtration rate was
approximately 8 mL/min, resulting in a filtration time of ~6 h for 3 L.
Fig. 3. Removal of NO−3 , F− and various toxic metals from water during pine
3.4. Filtration of inorganic contaminants xylem filtration.
High levels of ions such as NO−3 and F− in drinking water may 70% (with the exception of arsenic). Notably, chromium and copper
adversely affect the health of (mainly) young children, causing fluorosis were removed by > 99% (below detection limit). Additional filtration
and methemoglobinemia. Whereas toxic metals such as arsenic and lead experiments were carried out with varying concentrations of NO−3 and
may lead to long term neurological effects (Rocha and Trujillo 2019; Fu F− (from zero to 10 mg/L-N and 5 mg/L-F) and constant concentrations
and Xi 2020). Both group of contaminants are frequently detected at of metals, to test the impact of the ions on metals removal. Concentra
high levels in groundwater wells in Africa (BGS - British Geological tion range of NO−3 and F- was selected to cover typical groundwater
Survey, 2001; Gamar et al., 2021). Subsequently, experiments in this concentrations in Africa (Nayebare et al., 2014). Removal of NO−3 and F−
section aimed to (a) determine the capability of xylem to remove NO−3 , was negligeable in all experiments; whereas removal of metals remained
F− and relevant toxic metals from water and (b) identify the impact of constant at approximately >70% (arsenic ≥40%) and was not affected
NO−3 , F− concentration on the removal of toxic metals. by the concentration of NO−3 and F− (see Fig. S2 in Supporting
Fig. 3 presents filtration results of 200 mL tap water, spiked with Information).
NO−3 (5 mg/L-N), F− (1 mg/L-F) and different toxic metals (at initial A large number of publications already demonstrated the use of low-
concentration of 1 mg/L each). While concentration of NO−3 and F− only cost biomass-based adsorbents for metals removal from water (e.g. Bilal
marginally decreased following filtration, metals were removed by ≥ et al., 2022); however, these studies commonly employ pretreated
biomass material (grinded, chemically or thermally treated) in a batch
treatment configuration. This is the first time an intact xylem material
was applied, using a flow-through system configuration. Xylem com
prises of highly lignified cell walls that provide mechanical support to
the plant. Lignin is a complex phenolic polymer, consisting of a large
number of carboxyl and hydroxyl groups. These negatively charged
functional groups may bind to metallic ions through ion-exchange
mechanism (Fig. 4), and are likely responsible for the high sorption
capacity of the xylem (Ge and Li 2018). Arsenic appears in natural water
as arsenous or arsenic acid (Guma et al., 2021), which are either neutral
or negatively charged, hence its low removal rate by lignin (and sub
sequently by the xylem). The negligible removal and effect of NO−3 and
F− strengthen the ion-exchange hypothesis, since these ions are nega
tively charged and do not compete with metals of sorption sites.
Fig. 1. Maximum volume of saline water (0.9% NaCl) filtered for different-size
pine xylem piece.
4
N. Ibrahim et al. Groundwater for Sustainable Development 18 (2022) 100802
Table 3
Filtration results for the five natural water samples.
Water source E. coli removal (%) Average flow (mL/min) MVF (L)
Table 2
General quality parameters of the tested waters.
Water source pH Conductivity Alkalinity mg/L as CaCO3 TSS mg/L TOC mgC/L NO−3 mg/L-N E. coli cfu/mL
μS/cm
SW - 1 8 682 130 37.5 3.6 1.6 47
SW - 2 8.23 746 95 28.8 8.9 2.3 31
GW-1 7.8 457 260 < DL < DL 5.2 0
GW-2 8.2 456 217 < DL < DL 4.3 0
DL – Detection Limit; TOC – Total Organic Carbon; TSS – Total Suspended Solids.
5
N. Ibrahim et al. Groundwater for Sustainable Development 18 (2022) 100802
casing into which the plant xylem sample is inserted for proper sealing may take more than an hour, which means that the method cannot be
via this subsystem. The sample must be snugly fit into the center of the used for immediate drinking.
cone washer. The cone washer can be compressed by hand into the hole
in the bottom of the top threaded connection piece. This tightens the seal Declaration of competing interest
between the walls of the inner diameter of the cone washer and the
sample of plant xylem. The compression is facilitated by the angled cut The authors declare that they have no known competing financial
around the edge of the bore at the bottom of the top threaded connection interests or personal relationships that could have appeared to influence
piece, designed to match the taper of the cone washer for a tight fit. The the work reported in this paper.
external bottom threads of the top threaded connection piece can then
be fastened into the top internal threads of the tapped bottom piece. As
Acknowledgments
the parts are threaded together, the cone washer and bottom of the
sample of plant xylem bottom out on the ledge present inside the tapped
We would like to thank Zohara Bowker, Sara Hayun and Noa Levin
bottom piece created by the bore, further compressing the walls of the
for their work, and Aviv Kaplan and Dror Avisar for their help with
inner diameter of the cone washer around the sample of plant xylem.
metals analysis.
This results in the formation of a tight seal around the sample. The
bottom hole serves as the outlet through which water can exit this
Appendix A. Supplementary data
subsystem post-filtration.
The second sub-system is designed to provide a pressure of approx
Supplementary data to this article can be found online at https://doi.
imately 0.5 bar to the water, to force it through the plant xylem. This can
org/10.1016/j.gsd.2022.100802.
be done by multiple methods; for example, by using an elevation head or
with pressure provided by a weight. In the first option, the xylem holder
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