Adsorption of viruses onto surfaces in soil and water

~'tlt¢~r Resct~rch Voi. 9. •p 473 to 4xd,. Pergamon Press 1~'5. Printed in Great Britain.

ADSORPTION OF VIRUSES ONTO SURFACES IN SOIL AND WATER GABRIEL

BII-I'ON

University of Florida. Department of Environmental Engineering Sciences. Gainesville. Florida 3261 I. U.S.A. (Receired l March 1974)

IN-i'RODUCTION Viruses are electrically charged colloidal particles which may adsorb to surfaces outside the host cells. These sorptive interactions may have a strong influence on the behavior of viruses in their environment. The increasing pollution of our natural waters and the fact that viruses are important agents of human diseases have prompted research on their fate in water bodies (Berg. 1967). The occurrence of suspended solid particles, such as clay minerals, in natural waters probably exerts some influence on the behavior of viruses. Moreover. the removal of viruses by biological treatment processes involved in the purification of waste waters, is partially based on the adsorption of viruses by suspended solid particles. Soils contain a variety of colloidal particles including clay minerals and organic matter. Thus, the soil matrix offers a large active surface area which enables sorptive interactions to take place. The subject of sorptive interactions between soil particles and microorganisms has been reviewed by Marshall (1971) and Muller and Hickisch (1970). However, little attention was given to the adsorption of viruses by soil systems. This subject is of great importance when the movement of viruses through soils is under consideration and as means ofpreventing the pollution of our underground waters. Sorptive effects are also probably involved in the interaction between clay and organic matter and the spread of plant diseases by soil-borne viruses (Alexander, 1961). In the present review our purpose is to consider the physico-chemical mechanisms involved in the adsorption of viruses to biological and nonbiological surfaces and to stress the influence of these sorptive interactions on the behavior of viruses in their environment. I will also discuss the importance of the adsorption process in water pollution control and the concentration and purification of viruses.

MECHANISMS OF THE SORPTION BETWEEN VIRUSES AND SURFACES

Adsorption of viruses to host cells and to erythrocytes

Within the context of the present review, we shall confine courselves to a general outline of the basic features regulating the adsorption of viruses onto cell surfaces. More information on virus-cell interactions may

be found in the virology literature (Luria, 1953; Prier, 1966; Stent, 1963; Tolmach, 1957). Most of the studies dealing with virus-cell interaction use the bacteriophage--host cell model because it affords more accuracy in the quantitative measurements of the kinetics of this type of interaction. In order to infect host cells phages must become adsorbed to the bacterial cell wall. The adsorption obeys the first order kinetics and may be interpreted as a diffusion of the small viral particles towards the larger bacterial cells. As a result, nearly each collision between a virus particle and a bacterial cell results in virus adsorption (Delbruck, 1940). The adsorption rate increases with the number of host cells (Krueger, 1931) and the reaction is completed when the sorptive capacity of the host cells reaches saturation (Schlesinger, 1965). The adsorption process is greatly influenced by the presence of cations in the suspending medium. These cations help neutralizing the excess of negative charges on the surface of both the virus and host cell (Puck et al., 1951 ; Tolmach and Puck, 1952). Puck and his associates (1952) reported that monovalent cations were required in ten-fold higher concentrations than divalent cations. The optimum concentration of cations needed for maximum adsorption varies with the phage involved (Tolmach, 1957). In addition to inorganic salts, the adsorption of phages to host cells may require an organic cofactor such as tryptophan (Garen and Puck, 1951). The adsorption process involves specific chemical groups on the surface of both the virus and host cell. Thus, it was found that positively charged amino groups on T2 phage interact with negatively charged carboxyl groups on Escherichia coil B (Puck and Tolroach, 1954; Tolmach and Puck, 1952). As a result of this interaction the attachment of the bacteriophage to its host cell is suppressed at pH values at which the ionization of carboxyl and amino groups is inhibited. It has been proposed (Garen, 1954; Garen and Puck, 1951 ; Stent and Wollman, 1952) that the attachment of phages to bacterial cells consist of two steps: a first reversible step followed by an irreversible one characterized by temperature-dependent enzymatic transformations. The two-step adsorption of viruses somewhat resembles the attachment of marine bacteria to surfaces (Marshall et al., 1971 ; ZoBell, 1943). It was found that the adsorption consisted of two phases: a reversible

473

474

GABRIELBI'rTOX

phase followed by an irreversible one which was due to the production by the marine bacteria of polymeric substances which bridge between the bacterial cell and the glass surface (Marshall et al.. 1971). It has been demonstrated that specific components, extracted from the host cell walls, may adsorb phage particles (Imaeda and San Bias, 1969). Moreover, phage attach to the cell surface by their tail fibers (Anderson, 1953) whereas in the case of myxoviruses the receptors are distributed all over the surface of the virus particle. In certain cases, bacterial cell appendages, such as flagella, may act as adsorbent for phage particles (Meynetl, 1965). Viruses, notably myxoviruses, are able to adsorb onto the surface of red blood cells (Hirst, 1942). The ability of erythrocytes to retain viruses is called hemadsorption. This process allows a selective sorption of erythrocytes onto a monolayer of virusinfected host cells (Shelokov et al., 1958; Vogel and Shelokov, 1957). This has a practical advantage because it may serve as a reliable test for the diagnosis of some viral infections. Adsorption of viruses to other surfaces

Viruses are colloidal particles (20--200 nm) which are negatively charged at pH values close to neutrality. Their adsorption onto biological and nonbiological surfaces depends upon the nature of the adsorbent and upon the ionic composition and pH of the medium in which they are suspended (Pollard, 1953; Valentine and Allison, 1959): Valentine and Allison (1959) studied the adsorption of viruses and latex particles of similar size onto nitrocellulose, carbon, aluminum, and gold surfaces. It was shown that in a shaken system, the rate at which virus and latex particles come into collision with a surface can be predicted from the theory of Brownian motion. Except for the aluminum surface which is positively charged, the adsorption of the viruses onto surfaces was dependent upon the presence of cations (Na, Ca, AI) in the medium. An increase of the ionic strength of the medium led to a reduction of the thickness of the double-layer around the particles which came in close vicinity and were then bound by attractive forces, e.g. London-Van der Vaals forces. The adsorption of viruses onto various biological and nonbiological surfaces has been summarized in Table I. The implications of these sorptive interactions will be discussed in the last part of the present review. Activated carbon is a widely used adsorbent for the removal of organic materials from polluted waters. The ability ofactivated carbon to adsorb various types of viruses from water and waste water has been reported (Carlson et al., 1942; Cookson, t965; Fair et al., 1948; Neefe et al., 1947; Warner, 1967; Watson and Drewry, 1971). However, organic substances present in natural waters were found to compete with the viruses for the adsorption sites on the activated carbon (Sproul et al., 1967; Watson and Drewry,. 1971). The mechanism of adsorption has been studied in detail by Cookson (Cookson, 1965, 1967, 1969; Cookson and North, 1967), who used bacteriophage T4 as a model.

He showed that the adsorption process was reversible. obeyed the Langmir isotherm and was probably diffusion-limited. The attraction between the virus and the carbon was shown to be electrostatic in nature. Cookson proposed that, at neutral pH, positively charged amino groups on the viruses probably adsorbed to negatively charged carboxyl groups on the carbon particles. He also showed that the tail fibers of the bacteriophage played a significant role in the adsorption process. A large amount of information is available on the sorption of bacterial cells to clay minerals and other soil particles (Filip, 1973; Marshall, 1971). These sorptive interactions have important implications in the behavior of microorganisms in their natural habitats (Stotzky, 1967). Comparatively few studies have been made on the adsorption of viruses on clay minerals. Data are available in the literature on the sorption of viruses on kaolin (Filder and Kay, 1963), bentonite (Shyrobokov, 1972), activated attapulgite (Bartell et al., 1960), bentonite, vermiculite and pyrophyllite (Globa et al., 1971, 1972), and onto marine sediments containing clay minerals (Jakubowski, 1969; Roper and Marshall, 1974). Carlson et al. (1968) made a detailed study on the adsorption of bacteriophage T2 and type I poliovirus to kaolinite, montmorillonite and illite. It was found that the sorption of these viruses depended on the type and concentration of cations present in the water. Hence, a maximum level of adsorption required 10 times more monovalent Na ions than divalent Ca ions. The adsorption process was reversible and took only a few minutes. Desorption of the viruses occurred when the ionic strength of the suspending medium was lowered. However, Jakubowski (1969) reported that the viruses did not desorb spontaneously when they were resuspended in a medium of lower ionic strength. Roper and Marshall (1974) showed that the desorption of a bacteriophage from a marine sediment was moderate at the highest level of salinity, decreased with reduced salinity and then rapidly increased when the salt concentration was further reduced. The adsorption on clay minerals may be hindered or even reversed by the presence of proteinaceous materials such as egg and bovine albumin (Carlson et al., 1968) or fetal bovine serum (Jakubowski, 1969) in the medium. Clay minerals vary in their ability to sorb virus particles. A higher electrolyte concentration was required for montmorillonite than for kaolinite (Jakubowski, 1969). Carlson et al. (1968) found that under similar ionic conditions kaolinite and montmorillonite adsorbed a same amount of viruses. Howex;er, illite, because of its higher negative charge, required twice as much salt to attain a similar binding capacity. These authors concluded that the surface exchange capacity, determined by the surface charge density and clay particle geometry, was an important factor which governs the adsorption process. Difficulties are encountered when one attempts to show the virus adsorption sites by electron microscopy (Jakubowski, 1969). However, Roper and Marshall (1974) succeeded in showing an

Adsorption of viruses onto surfaces in soil and water

Table 1. Summary of the literature on the adsorption of virus particles onto surfaces Adsorbent

Virus adsorbed

Reference

I. Activated carbon

Bacteriophage (T 4 and fZ)

Cookson (1965. 1967, 1969, 1970) Cookson and North (1967) Watson and Drewry (19-/I)

Infectious hepatitis virus

Carlson et ai. (194Z) Warner {[967)

T h e i l e r ' s virus

Fair~al.

Z.

Glass

(1948)

T 2 bacteriophage

Shepard and Woodend (19~[)

Influenza and adenoviruses

Boche and Quilligan (1966)

).

Celite (diatomaceous siiicon dio.x/de )

Rous Sarcoma virus

Riley (1948)

4.

Aiumine

Bacteriophage (T z )

Shepard and Woodend (1951)

5.

6.

Precipitable s a l t s

Polyelectrol},tes

7. Clay minerals

8. Silicates other than

Influenza virus

D r e s c h e r (1960, 1961}

Pollovirus

Sabin (1932)

Poliovirus

SprouletaL

Various viruses

L a u tie r et al. (1971} Moore e~"al.'~(1970) T a v e r n e et ah (1957) Wallis an-d'~elnick (1967a, 1967b)

Bacteriophage (T 4 and MS2)

ChandhurF and Engelbrecht (197Z) T h o r u p e ~ a h (1970)

E nteroviruses

Thorup et al, (1970) Wallisetal. (1970, 1971)

Tobacco mosaic virus

Johnson et al. (1967)

(1969)

Bacteriophage (T71

F i l d e r and Kay (196)) Roper and Marshall (1974)

Poliovirus

Bartell et al. (1960) Ca r Is onet--a-1. (1968) Globa et'aL (1971) J a k ub o-~s-~y (1969)

C oxsackie virus

Shyrobokov (1972)

Poliovirus

Lo (19-/0)

Bacteriophage (T7)

Wentworth (1968)

Bacteriophage

Dieterich (1953)

Cytoplasmic polyhedrosis virus

Hukurnara and Wada (197Z)

Bacteriophage (f21

Reece (1967)

Pla nt v i r u s e s

Murphy and Syverton (195fl)

Bacteriophages (T I, T z, fZ)

Puck and Sagik (1953) Watson and Drewry (1971)

In/luenza virus

Muller and Rose (1952) Puck and Sagik (1953)

Poliovirus

Lo Grippo (1950)

clay m i n e r a l s

9. Sand 10.

I1.

Soi_._.!l

lon excl~tnge r e s i n s

IZ. Iron oxides

13.

Membrane f i l t e r s

Bacteriophage (T7)

Bitton and Mitchell (1974a)

Hnte r ovir us

L a t i n and G a l l i m o r e (1971) Rao et al. (1968) Warr'een'--e_~tal_~ (1966)

Pollovirus Type 2

Hechrnat (1972)

E n t e r o v i r us

Cllver {1965, 196"/, 1968) Wallis and Melnick (1967a, 1967b)

475

176

GABRIELBtTTON

electron micrograph of Escherichia c o l i - b a c t e r i o p h a g e sorbing onto montmorillonite either in a face to face or tail to face orientation on the surface of the clay. Silicate minerals have been investigated for their ability to sorb viruses. Wentworth (1968) described the adsorption of T.~ bacteriophage on silicate particles surface in relation to pH and mobility of the suspended particles. Lo (1970) reported the adsorption of type I poliovirus onto silicate minerals such as actinolite, enstatite, microcline, olivine, and sillimonite. The attachment of the poliovirus to these minerals was hindered by the presence of egg and bovine albumin and reached values of 64-90 × 10"~virus particles adsorbed per mg of silicate. Information about the sorption of viruses onto sand particles is of practical significance since the use of sand filters is a current practice in water pollution control. When compared to clay minerals, sand is relatively a poor adsorbent because of its small surface area. Dieterich (1953) conducted a series of experiments on the behavior of a bacteriophage in sand filters. It appeared that sand removed viruses mainly by adsorption which results from electrostatic attraction between sand and virus particles. As reported for activated carbon and clay minerals, egg albumin competed with the bacteriophage for the limited amount of active sites on the sand. Since viruses behave as proteins. Filmer and Corey (1966) studied the movement of virus-sized albumin particles through sandy soil columns. It was shown that adsorption played an active role in the removal of the protein. Little attention has been given to soils concerning their sorptive capacity towards viruses. Three out of four soils studied by Reece (1967) displayed a high sorptive capacity towards bacteriophage f2. The adsorption was reversible, was conform to the Freunlich isotherm, was more or less pH dependent and directly related to the surface area of the soil. Undoubtedly no quantitative conclusion could be drawn due to the small number of soils studied. Because of this limitation, no attempt was made to determine whether there was any correlation between the sorptive capacity and other properties of the soil such as clay or organic matter content. The importance of entomogenous viruses as successful microbial control agents has led some investigators to study their persistence under field conditions (Hukuhara and Wada, 1972; Jaques, 1969; Yendol and Hamlen, 1973). Tests on the adsorption of cytoplasmic polyhedrosis virus on a volcanic ash soil showed that the process increased with soil acidity but decreased when the soil was amended with reagents such as pyrophosphate, EDTA, oxalate or fluoride (Hukuhara and Wada, 1972). Ion exchange resins have been used as models for the host cell surface when one considers the principles governing the attachment of viruses to host bacterial cell walls. The functional groups on the surface of the resin affect its binding ability. Many authors reported the adsorption of viruses onto cationic (Muller, 1950; Muller and Rose, 1952; Puck and Sagik, 1953) and anionic exchange resins (Kelly, 1953; Lo Grippo, 1950;

Muller, 1950: VCatson and Drewry, 1971). A detailed study was undertaken by Puck and Sagik (1953) on the adsorption of Tt and 7-_, bacteriophage, and of influenza virus on cation (Nalcite RCH) and anion (Dowex I) exchange resins. At pH 7 when some of the T-phages are negatively charged (Putnam. 1950), Tt and T.,. suspended in distilled water, readily adsorbed to the anionic resin but failed to do so with the cationic resin. The attachment of the phages to the cationic resin occurred only in the presence of enough cations to neutralize the negative charges on both the resin and the virus. It was also found out. that Tt and T., differed in their ionic requirement for an optimum sorption on the resin. A mammalian virus, such as influenza virus, behaved in a manner similar to that of the phages. Interestingly, 7-_,was split into its DNA and protein components as a result of its attachment to the cationic resin. Watson and Drewry (1971), working with 1; bacteriophage, showed adsorption to an anion exchange resin. The process was hindered by the presence of organic matter in the medium. Iron oxides have been used as adsorbents for the removal and concentration of viruses. Influenza virus was reported to be strongly adsorbed by hematite (Warren et al., 1966). A magnetic iron oxide displayed an excellent ability for adsorbing a variety of viruses (Rao et al.. 1968). Magnetite (Fe304) has also been used as an adsorbent for bacteriophage T; in the presence of calcium chloride (Bitton and Mitchell, 1974a). The desorption of viruses from iron oxides is easily attained through the use of 10% sodium phosphate (Warren et al.. 1966), 3~o beef extract or foetal calf serum (Rao et al.. 1968) at pH 8. Although the experimental conditions differ, Table 2 shows that the virusadsorbing capacity of the magnetite used by Bitton and Mitchell (1974a) is similar to that of the magnetic iron oxide studied by Rao et al. (1968). Hematite appears to be less efficient. The adsorption of viruses onto iron oxides is a physical process which is slightly dependent on temperature (Rao et al., 1968). However, Warren et al. (1966)reported that the number of viruses adsorbed onto hematite increased 2--4 fold when the temperature was increased to 37-'C. Therefore, a better understanding of virus adsorption on iron oxide is necessary. Various types of viruses attach to glass and oxides of silicon and aluminum. The adsorption of bacteriophage (Puck et al.. 1951 ; Shepard and Woodend, 1951) to the electronegative surface of glass is affected by the salt concentration, pH, and organic content of the suspending medium. By immersing microscope cover slides into a suspension of labeled viruses, Boche and Quilligan (1966) were able to test the sorption of influenza. A virus and adenovirus type 6 on glass treated with silicon and paraffin. Silicon decreased the adsorption of both types of viruses, whereas paraffin led to an enhancement of the sorptive ability of the lipid conmining influenza virus which has more affinity towards paraffin. Celite, a diatomaceous silicon dioxide, binds to Rous sarcoma virus (Riley, 1948) and bacteriophage 7"2(Shepard and Wooden& 195 I) in the presence of the

Adsorption of viruses onto surfaces in soil and water

477

Table ..~ Adsorption of viruses onto iron oxides Ads°rpti°n(l ) (virus particle/g)

References

Iron Oxide

Virus

Hernat:te {Fez031

Infiuenza virus ( P . R . 8)

Magnetic iron o x i d e (M0 Z53)

Coxsackie virus A-3

8 "¢ 10s

R a o e t ai. lqb$---

Magnetite Fe304

Bacteriophage T7

Z v 107

Bit'ton and Mitchell, 1974a

10 )

W a r r e n e~t al_.~ (1966)

(1)The n~trnber of viruses adsorbed per g of iron oxide were estimated from the references cited in the table.

appropriate concentration of sodium chloride. Cab-OSil, the trade name for colloidal SiO2, is also a good adsorbent for viruses (Boche and Quilligan, 1966). AI.,O3, a positively charged material, is known for the attachment of bacteriophage T, (Shepard and Woodend, 1951), poliovirus (Sabin, 1932) and influenza virus (Drescher, 1960, 1961). According to Dreseher (1960, 1961) the adsorption of influenza virus onto aluminum oxide obeys the Freunlich isotherm, is reversible and does not show any change between pH 6.1 and 7.8. Preformed floes of aluminum hydroxide, aluminum phosphate and calcium phosphate are successful adsorbents generally used for the concentration and isolation of a great variety of viruses (Lautier et al., 1971 ; Sproul et al., 1969; Taverne et al, 1957; Wallis and Melnick, 1967a, 1967b). Synthetic insoluble polyelectrolytes are commercially available polymers and are used in water and waste water processes. P.E. 60, a crosslinked copolymer of isobutylene maleic anhydride, has been studied for the adsorption of viruses from water 0Atallis et al., 1969, 1970, 1971). Enteroviruses, rheoviruses, and adenoviruses are readily adsorbed to P.E. 60 at low pH (3.0-4.5) and are easily eluted from the adsorbent at pH 8-9 (Wallis et al., 1971). Johnson et al. (1967) reported a 100% adsorption for tobacco mosaic virus and 99.9Vo for poliovirus. They were able to desorb those viruses from the synthetic polymer by using a 1 M solution of sodium chloride. Cationic polyelectrolytes generally display a higher sorptive capacity than nonionic or anionic polyelectrolytes (Chaudhury and Engelbrecht, 1972; Thorup et al., 1970). Thorup et al. (1970) explained this phenomenon by suggesting that cationic polyelectrolytes bear positively charged amino groups which attract the negatively charged virus particles. The adsorption was affected by the ionic strength of the medium and was depressed in the presence of very high or very low salt concentrations. The lower binding capacity, under higher ionic conditions, was probably due to the contraction of the polyelectrolyte molecules (Priesing, 1962). Membrane filters, composed of cellulose derivatives, are commonly used in many laboratories for the sorp-

tion of viruses from contaminated suspensions. Membrane-adsorption techniques have been discussed in detail by Hill et el. (1971). Fundamentally, the adsorption of viruses onto membrane filters is affected by factors such as the chemical nature of the membrane, ionic composition of the suspending medium, pH, and the presence of interfering organic substances in the medium. Nicoli et al. (1964) compared the adsorption of Myxovirus parainfluenzae I (sendal virus) on cellulose, paraaminobenzylceUulose (PABC), diazobenzylcellulose (DCB), diethylaminoethylcellulose (DEAEC) and cellulose on which the mucopolysaceharide of bovine submaxillary gland has been fixed (MDBC) by diazotation. The virus attached to all the types of cellulose except to cellulose and PABC. Cliver (1968) showed that cellulose nitrate membranes have more affinity for viruses than cellulose triacetate membranes. The binding of viruses to membrane filters is enhanced by the presence or addition of divalent cations to the suspending medium (Hechmat, 1972; Rao and Labzoffsky, 1969; Wallis and Melnick, 1967a and 1967b) but is adversely affected by the presence of organic substances which compete with the virus on the membrane adsorption sites (Cliver, 1965 and 1968; Moore et al., 1970; Wallis and Melnick, 1967a). Moreover, the sorption capacity of the membrane is markedly enhanced by reducing the pH toward the isoelectric point of the virus (Wallis and Melnick, 1967a). The principles discussed above are applied for the desorption (elution) of viruses from membrane filters. For example, an efficient elution will be obtained at a high pH, e.g. pH 8, with a proteinaceous substance, such as bovine serum or beef extract, as the eluent. IMPLICATIONS O F T H E SORPTIVE I N T E R A C T I O N S B E T W E E N VIRUSES A N D S U R F A C E S IN SOIL A N D W A T E R

Use o f adsorbents in water pollution control

Viruses, mostly from human and animal fecal origin and from industrial wastes, find their way into the waterways and are potential disease transmitters. It is, therefore, of utmost importance to find suitable water treatment procedures for the removal of the virus

478

G A B R I E L BITTON

Table 3. Removal of viruses by adsorption in water treatment processes

ADSORBENT

(Number

VIRUS o£ p a r t i c l e s / n ~ l )

REMOVAL ~"

R E .%LAR K S O N THE PROCESS

REFERENCE

Bat ch s t u d y

Sprottl et al.

Activated carbon N u c h a r C-190

( 0 . 2 5 g / 1 0 0 ml)

Activated c a r b o n (25 m g / L )

T 2 bacterioohage (75 >e 10 ~)

75

T 2 bacteriophage (75)¢ i0 ~)

9

Continuous flow experiment ( 122 1 / m i n / r n 7')

Sproul et al. (1969}

P o l i o v i r u s Type l

25

Continuous f l o w exveriment ( 12 Z i/rnin/.'rt 2 )

S p r o ~ et at.:. (1969)

Infectious h e p a t i ~ s

A0

Conabination with

N e e f e et al. ( 194 7)

(1969)

flocculation

Polyelectrolytes

P u r i f l o c CjZ ( l i n g / L }

T 2 bacteriophage

98

Cornblned with a l ~

(40ppm) flocc ulation

Thorup et al. (1970)

Purifloc C3Z ( i r n g / L )

Type l poliovirus

81

Cort~bined with a l u m (10pprn) floc culation

Thorup et al. (1970)

Prirnafloc C 7 (ling/L)

T 4 bacteriot~hage (4.5 ~ l0 ~)

99.9

C o m b i n e d with a l u m (50pprn) flocculation

C h a u d h u r y and Engelbrecht (197Z)

Styrene-malel¢ anhydride copoIyTne r

Type I poltovirus

99. 9

Adsorption in the presence of NaCI

Johnson et al. (1967)

,r Sand filtration (coal and sand £ilter)

Type I polLovirus (2 ~ I0 ~)

up to 98

F l o w r~te: 2-6 g p m / s q . ft. Aluna added ahead

Robeck e...~tal__: (1962).

of the f i l t e r

Stabilization pond (suspended solids: 1030mg/L)

Sobsey and C o o p e r (1973)

T y p e I pol~ovirus (3 ~ I0 ~)

30

T h e a d s o r p t i o n to s o l i d s o b e y e d the Freunlich isotherm

C o x s a e k i e virus

67

T h e a d s o r p t i o n to s o l i d s C l a r k e e t al_~. o b e y e d the F r e u n d I i c h (1961) isotherm

T 7 bacteriophage (14 Y 10 )

98

Water seeded w i t h magnetite in the presence o£ CaCl 2 and poured through a f i l t e r p l a c e d in a zxtagnetic field

Activated Slud~e P r o c e s s

Isuspended solids: 2320 nag/L)

Magnetic filtration ( m a g n e t i t e : 500 r a g / L )

hazard from water and waste water. Unfortunately, no system entirely removes virus particles from water. The processes generally used involve storage, biological filters, flocculation, stabilization ponds, activated sludge, sand filtration, activated carbon, and disinfection procedures such as chlorination, bromination or ozonation (Committee on Env. Qual. Manag., 1970; Grabnow, 1968; Nupen, 1970; Poynter, 1968; Sproul, 1972). However, according to Sproul and his coworkers (1969) the most important mechanism involved in the removal of viruses in waste water treatment plants is the adsorption process. Therefore, we will deal only with methods involving the use of adsorbents. These methods are summarized in Table 3. The data show the extent of removal of viruses in batch and continuous flow studies. It is clear that activated carbon remove viruses quite poorly, especially enteric viruses

Bitton and M i t c h e l l

(1974a)

(Neefe et al., 1947; Sproul et al., 1967, 1969). Therefore, this adsorbent does not play a major role in virus removal from water. Recently, attention has been given to cationic polyelectrolytes used as prime coagulants or as coagulant aids in association with alum or ferric sulfate (Chaudhury and Engelbrecht, 1972; Johnson et al., 1967; Thorup et al., 1970). Their use undoubtedly provides an effective and inexpensive means of removing viruses. Although sand is a poor adsorbent (Dieterich, 1953), sand filtration, intelligently combined with alum flocculation and operated under slow flow rates (Robeck et al., 1962), removes significant amounts of viruses. Few studies have been made on the removal or inactivation of viruses in stabilization ponds (Christie, 1967; Malherbe and Strickland-Cholmley, 1967). The study of Sobsey and Cooper (1973) showed that, apart from viral reduction due to microbial activity in an algal-bacterial treatment system, adsorption of

Adsorption of viruses onto surfaces in soil and water poliovirus to solids played a role in their reduction in waste waters. In the activated sludge process, the adsorption mechanism was also found to influence the reduction of type I poliovirus and coxsackie virus in wastes (Clarke et al., 1961). However. in their study, the virus--sludge complex appeared to be very stable and to lead to a poor recovery of the viruses from the sludge. Although clay minerals have been proposed for use in water purification (Globa et al., 1971, 1972), their sorptive behavior towards viruses in natural water is temporary and is readily hindered by organic materials normally present in these waters (Carlson et al., 1968). Finally, magnetic filtration, which consists of seeding virus-contaminated water with colloidal magnetite and pouring the mixture through a filter placed in a magnetic field, has been used for the removal of bacteriophage T7 (Bitton and Mitchell, 1974a). This process deserves further investigation on its applicability in plant scale tests and on its economic feasibility. Because of the increasing demand for potable water and also because of the considerable attention given to the direct reuse of waste waters, more investigations, notably field tests, are needed for the improvement of the existing water treatment procedures. More effort should be given to research dealing with virus removal by filtration based on adsorption and by commercially available cationic polyelectrolytes. Sorptive interactions in soil systems

Because of their sorptive properties, soils possess the ability to retain pollutants of chemical and microbial origin. Undoubtedly, the adsorption of viruses to soil particles is significant and readily influences both the movement of viruses through soil columns and their survival pattern. Until very recently little was known about the movement of viruses with percolating water. This type of study is of great importance, because of reports of outbreaks of hazardous viruses, such as the infectious hepatitis virus, which pass through the soil and contaminate the ground-water supplies (Mosley, 1959; Clarke and Chang, 1959). Viruses are known to be more resistant to chlorine than bacteria. Therefore, their behavior in soil systems is of great importance to health authorities. Soils appear to be able to remove bacteria (Bitton et al., 1974; Muckel, 1950; anon., 1953) and viruses by physical means such as straining and adsorption. However, because of the smaller size of viruses, adsorption may play the major role in their removal (Drewry, 1969; Drewry and Eliassen, 1968; Eliassen et al., 1965; Hori et al., 1970; Reece, 1967; Tanimoto et al., 1968). A summary of the literature on the movement of viruses through various soil systems is shown in Table 4. Depending on the nature of the soil and the underlying strata, soil percolation may or may not aid the process of water purification. Gilcrcas and Kelly (1955) compared the movement of Coxsackie virus, bacteriophage and Escherichia coil through columns packed with a garden soil. It was found that even 3 ft of such soil were ineffective in removing the viruses. Unfortunately, this

479

study did not reveal the effect of factors such as flow rate and soil type. Laak and McLean (1967) reported that poliovirus type 3 was not eliminated by percolation through medium sand, sandy loam or a garden soil. The domestic water supplies of Honolulu and Oahu island are pumped mainly from the groundwater body (Hori et al., 1970). Despite the adsorption ability of two Oahu soils towards a bacteriophage (Tanimoto et al., 1968) and poliovirus type 2 (Hori et al., 1970) the breakthrough of these viruses was observed. Hori et al. (1970) concluded that the possibility of pollution of ground-water does exist, especially when the stratum underlying the soil is interrupted by fissures or fractures which probably help in the channeling of the viral contaminant to the ground-water supply. Other researchers (Drewry, 1969; Drewry and Eliassen, 1968; Eliassen et al., 1967; McGauhey, 1968, 1971; McGauhey et al., 1966) stated that virus movement through a continuous stratum of common soft should present no great hazard with respect to underground water supplies. These conditions are strengthened by the results of the Santee, Calif., Project, which has shown that viruses are removed in less than 200 ft travel through a sandy gravel bed (Merrel and Ward, 1968; Merrel et al., 1965; anon., 1965). Romero (1970), summarizing the subject of the movement of bacteria and viruses through porous media, concluded that viruses do not migrate more than 200 ft from the source of contamination. Other areas of research, such as biological control of insects by entomogenous viruses, are concerned with the fate of these viruses when they reach the soil surface. Insect viruses, sprayed on plant leaves for biological control purpose, are washed by the rain and reach the soil ultimately (Yendol and Hamlen, 1973). Studies have shown that these viruses, which are readily adsorbed onto the soil, do not migrate below a depth of 5 cm and, therefore, infect the soil for long periods (Hukuhara and Namura, 1972; Jaques, 1967a, 1967b, 1969). These studies have practical implications since the sorbed viruses may reinfect the leaves through the action of wind or splashing rain. The spread and survival of viruses in the soil environment are probably greatly affected as a result of ' the adsorption of viruses to soil particles. In soil systems there is a lack of information concerning the mechanism of survival of viruses adsorbed to soil particles. Most of the research has been undertaken in the area of plant pathology since many phytopathogenic viruses may be soil borne and/or soil transmitted. These viruses are adsorbed by the clay fraction of the soil and remain viable for many years (Thung and Dijkstra, 1958; Van der Want, 1951). Myamoto (1959a, 1959b) investigated the mechanism of transmission of soil-borne plant viruses. He showed that the infectivity of the clay fraction of the soil was much higher than that of the coarser fraction. He proposed that the clay particles may act as carriers for plant viruses. These viruses, as a result of their adsorption to soil colloids, are protected from adverse environmental factors (David and Gardiner, 1967; Murphy et al., 1958) and

480

GABRIEL BITTON

Table 4 Movement of viruses through soil columns

Soil

V i r u s type ~C)neentration ~f r~he feed suspension in pfu/nnll

9 t y p e s of s o i l s

Tl,

T 1 and ~ -

bac~erlo hages (7. ? ~ l ~ to 4. 3 ,x 107~

3 types of Oahu s o i l s (Hawaii)

Flow ~ate

0. 0 7 8 - 0 . 313

Distance of t r a v e l

Comment

on ..irus

adsorption

45-50 cm

All the coiurr.nJ r e m o v e d o v e r 99 g

0. 5-6 in

96. 6 - 9 9 . 34 r e m o v a l

6-15 in

22-35~ r e m o v a l

2. 5 and 6 in

100g a d s o r p t i o n

Tanimo~o e t at....= (1968}

rnl/min

Poliovlrus type 2

Dre~-ry and E l i a s s e n (1968~

Hori e_~al_~ (1970) 7. 9 and 10. 5 mi/miu

Wahiawa and Lahaina (low hurnic l a t a s o l s ~

Reference

T a n t a l u s cinder (gratxular m a t e r i a l so il)

3 types of Oahu soils, H a w a i i (Same as a b o v e l

T bacte iophage (~..5 × l0 t )

Garden soil

C o x s a c k i e v i r u s and bacteriophage T 4

6, 18, and 36 in

S o m e reduction of n u m b e r of viruses was attained in the 36 i n column

Gilcreas and

Poliovirus-3

] 2 c m for m e d i u m sand 14 c m for garden soil and s a n d y loam

P o l i o v i r u s was not e l i m i n a t e d by f i l t r a t i o n through t h e s e s o i l s

Leak and M c L e a n (19671

M e d i u m sand, g a r d e n s o i l and sand~f l o a m s o i l

(Same as above)

Kelly (1955)

Ottawa sand

Bacteriophage active a g a i n s t S. p y o s e n e s v a t . albus

ZO, 3 m l / m i n and 3Z. 5 m l / m i n

34 c m

A d s o r p t i o n not affected by the flow rate

D i e c e r i c h (1955)

Ottawa sand

P o l i o v i r u ~ type I (38 ~" l 0 ;b ~o 15. 3 w I0 ~}

I / I Z g to Z g p m / $ q , ft.

Z ft.

Adsorption increased when the flow rate decreased

Robeck e tt al...~. (196Z)

Sandy gravel

Polio vaccine virus type )

Wells situated 200 and 400 ft. downstream

Effluents n e g a t i v e for pollovlrus

Santee proiect Santee fUtratlon study ([q65}; M e r r e l and Ward (1968} M e r r e l eft al..._:

(1965}

(Smith and Courtney, 1967), cholesteriol columns (Younger and Noll, 1958), and precipitable salts such as aluminum hydroxide or calcium phosphate (Wallis and Melnick, 1967c, 1967d). Comparative data dealing with the use of adsorbents in the concentration and recovery of viruses are given in Table 5. Although considerable progress has been made in recent years in the field of concentration techUse of adsorbents in the concentration and purification niques, there is still a need for a general method which of viruses would be simple, efficient, of low cost and suitable for One of the major difficulties encountered in the a broad range of viruses and various qualities of water. detection of viruses is their usual low concentration in From Table 5 it is clear that polyelectrolytes hold good water bodies. Therefore, a number of methods have promise for routine use in the future. The membranebeen proposed for the concentration of viruses from adsorption technique, although costly in certain cases, very dilute suspensions (Committee Env. Qual. Mana- is also promising and has been recommended by the gement, 1970; Hill et al., 1972; Shuval and Katznelson, Committee on Environmental Quality Management 1972). However, within the context of the present (1970). The iron oxide column technique is sometimes review, we shall deal only with methods based on the inconvenient because of the clogging of the iron oxide adsorption of viruses to particulate material. These bed with suspended material. Therefore, it is sometechniques involve the use of membrane filters (Cliver, times necessary to prefiltrate the water before passage 1968; Moore et al., 1970; Rao and Labzoffsky, 1969; through the column. Cholesterol, used as a concentratWallis and Melnick, 1967a, 1967b), polyelectrolytes ing adsorbent in small columns, presents the advan(Pana, 1971 ; Wallis et al., 1969, 1970, 1971, 1972), iron .tage of being injectable, non-toxic and nonantigenic. oxides (Rao et al., 1968; Warren et al., 1966), cellulose Thus, the attached virus particles along with the adsorderivatives (Nicoli et al., 1964), ion exchange resins bent may be resuspended and injected directly (Muller and Rose, 1952), passive hemagglutination (Younger and Noll, 1958). Another consideration is the are made unavailable for plant adsorption (Murphy and Syverton, 1958). Therefore, it is expected that heavy soils will retain their infectivity for longer periods than sandy soils (McKinney, 1946). More research is needed to determine the mechanism of protection of viruses by mineral and organic colloids in soil and other environments (Bitton and Mitchell, 1974b).

481

Adsorption of viruses onto surfaces in soil and water Table 5. Use of adsorbents in the concentration and recovery of viruses

Adsorbent

V~rus ~-?e (L~/luent c o n c e n t r a t i o n in ~nits/vol)

Polvele¢~rolvte '(P~'60) '

T y p e I polio~rus (2. I Z/rnl)

Cellulose m e m b r a n e s

Volu.~.e of 5 a.~. p l e (liters)

Concentration ~a¢'.or

£ recove:y

Reference

I~.00

i000-

35-~0

;Vallis et al. [i~7~) ---

Entero'eiruses

0. I

S0-I00

I00

%ValIis and .'xlelz!ck (1967a)

S e w a g e viruses (2. 5 - 1 8 4 / l i t e r )

3.8

--

100

Wallls and X[e',aick (1967b)

Type r oUovirus 1Z~-44/~00 rnl)

0.5

--

53-100

Iron O x i d e C o l u m n

C o x s a c k i e virus A - 9 (100/500 rnl)

0, 5

8

82

R a o et a l . (I~6~)

Aluminum

Variotts types of viruses (100/liter}

l

..

80"

V/al~is and .%Ielaick [1967c; 1967d)

hvdroxlde

Caeion exchange r e s i n

Influenza virus

0. I

Cholesterol C o l u m n

Influenza virus (160/rrd)

0. 139

R a o and Labzoffsky (1969(

8-16

--

Muller arid Rose (1952)

10

--

Y o u n g e r and .Noll (1958}

quantity of water being treated. The polyelectrolyte demand for potable water, more research is needed adsorption method allows the treatment of samples for the development of an efficient and inexpensive over 300 gallons of water whereas the aluminum hy- process for the removal and concentration of these infective particles. More attention should be given to droxide technique is limited to smaller volumes. Ion exchange resins have been mostly used as means studies dealing with the effect of adsorption of viruses for purification of viruses. The methods involved con- upon their survival and movement in soil systems. The ability of viruses to sorb to solid particles has sist in separating virus particles from nitrogenous materials, such as serum, in which they are suspended. found practical applications in other areas of research Hence, influenza virus has been purified by passage such as the one involved with the treatment of enteric through a cation exchange resin (Muller, 1950; Muller disturbances of viral origin (Martin, 1955). A clay and Rose, 1952; Puck and Sagik, 1953). Poliomyelitis mineral, attapulgite, was found to be superior to kaolin virus, poured through an anion exchanger, was for the adsorption of alkaloids (Barr and Arnista, adsorbed onto the resin along with nitrogenous mater- 1957), Staphylococcus aureus (Barr, 1957) and enteroials. Then, the virus was selectively eluted with a 10% viruses such as poliovirus, echo and coxcackie virus solution of dissodium acid phosphate (Lo Grippo, (Bartell et al., 1960). These results open the possibility 1950, 1952). Warren et al. (1966) reported that myxo- of using activated attapulgite as an adsorbent for the viruses, such as the PR8 strain of influenza virus, may treatment of various enteric disturbances. be partially purified by using hematite as adsorbent. Similarly, parainfluenza I virus (Sendai virus) has been highly purified by adsorption to diethylaminoethylcelREFERENCES lulose followed by elution with 0.5 M NaCI (Nicoli et al., 1964). Stephan and May (1968) proposed that the Alexander, M. (1961) Introduction to Soil Microbiology, serum treatment with adsorbents such as colloidal silliJohn Wiley, N.Y. cic acid could be used for the preparation of hepatitis- Anderson, T. F. (1953) The morphology and osmotic properties of bacteriophage systems. Cold Spring Harb. free sera. PR8 strain of influenza virus has been effiSyrup. quant. Biol., 18: 197. ciently separated from serum proteins by passing the Anon. (1953) Waste water reclamation in relation to ground virus suspension through a cholesterol column water pollution. Publ. no. 6, Calif. State Wat. Pollut. Bd. (Younger and Noll, 1958). Anon. (1965) Santee filtration study. A study of sewage effluent purification by filtration through natural sands and gravels of Sycamore Canyon, at Santee Bureau of Sanit. Eng. Dept. Publ. Hlth. GENERAL CONCLUSIONS Barr. M. 0957) Adsorption studies on clays II: the adsorption of bacteria by activated attapulgite, halloysite and We have shown the sorptive interactions between kaolin. J. Am. pharm. Ass. Sci. Ed., 46: 490-492. viruses and surfaces and their influence on the behavBarr, M. and Arnista, E. S. (1957) Adsorption studies on ior of viruses in soil and water environments. The presclays I: the adsorption of two alkaloids by activated ence of solid particles in natural waters undoubtedly attapulgite, halloysite and kaolin. J. Am. pharm. Ass. Sci. Ed., 46: 486-490. affects the survival and removal of viruses. The use of suitable adsorbents in water treatment processes was Bartell. P., Pierzchala, W. and Tint, H. (1960) The adsorption of enteroviruses by activated attapulgite. J. Am. shown to be indicated in the removal, concentration pharm. Ass. Sci. Ed., 49: 1-4. and purification of viruses. However, because of the in- Berg. G. (1967) Transmission o f Viruses by the Water Route creasing pollution of our natural waters and the higher (Edited by Berg, G.), Interscience, N.Y.

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