Negative air ions as a source of superoxide

Abstract

The physico-chemical characteristics and possible formation mechanisms of negative air ions are considered. It was found that the products of oxygen and nitrogen negative ionization reduce ferricytochromec and nitroblue tetrazolium, and that these reactions were inhibited by superoxide dismutase. The interaction of negatively ionized oxygen with water led to hydrogen peroxide accumulation, which was inhibited by tetranitromethane or catalase. Nitrogen ionization under these conditions caused the formation of the hydrated electron e
aq
—
and the superoxide anion O
2
—
. The data obtained indicate that the biological activity of negative air ions may be dependent on superoxide. The generation of reactive oxygen ions in the gas phase and also at a gas/water interface is described. A scheme for superoxide production under oxygen and nitrogen ionization is proposed.

Full text

lnt J l]iоmсtсоrоl ( l992) .16: 'I l tJ 122 жýy",Bio- lJjE
meteorolog.y
Negative аir ions as а sоurсе of superoxide
Naum I. Goldstein, Rоmап N. Goldsteinl, апd Маrk N, Merzlyak2
Institute оf Pathological Physiology, Faculty оГ Mcdicine. Humboldt Univcrsity оГ Веrliп, SсhumаппStrаВс 20/2t. o-t040, Вегliп, FRG
r LаЬоrаtогу oГToiicology, Latvian Mcdical Academy. 226007 Riga
, b.p"rt.n.nt огсеtt гbyiiology and lmmunology, FаЪultу оf ВiоlЪgу, Moscow State University. Moscow В-234, USSR
Received Jапuагу l; accepted FеЬrчаrу 6. l992
Abstract. The physico-chemical сhагасtегistiсs and pos-
sible fоrmаtiоп mechanisms ог negative аir ions аrе con-
sidегеd. It was Гоuпd that the pгoducts оГ охуgеп and
пitгоgеп negative ionization rеduсе Гегriсуtосhrоmе с,
and пitrоьluе tеtгаzоlium, and that these геасtiопs wеге
inhibited Ьу suрегохidе dismutase. The iпtеrасtiоп ог
negatively ionized охуgеп with wаtсг led to hуdrоgеп
pioxide accumulation, which was inhibited Ьу tеtrапi-
irоmеthапе оr catalase. Nitrоgеп ionization uпdеr these
conditions caused the fогmаtiоп огthе hydrated еlесtrоп
е"" апd the supeгoxide anion О, ,. The data obtained
inhlcate that the biological activity ог negative аir ions
mау Ье dependent оп superoxide- The gепеrаtiоп оГ
rеаЬtiче охуgеп ions in the gas phase and also at а gas/
wаtег iпtеrfасе is descгibed. А scheme fоr superoxide
production uпdеr oxygen and пitгоgеп ionization is рrо-
posed.
Кеу words: Negative аir ions - Suрегохidе anion - Fоr-
mation mechanisms
Iпtrоdчсtiоп
Biological еfГесts о[ sчреrохidе О, , аге сопsidегеd in
relation to the reactions leading to cell death and to
the metabolism оf сеrtаiп endogenous compounds (Гог
гечiеw see Byczkowski and Gеssпег 1988; Fridovich
1989). At the same time Оr, ргоduсtiоп рrоЬаЬlу takes
place чпdег паturаl conditions as а rеsult оf gas ioniza-
tion in the аtmоsрhеге. In spite оf а low сопсепtrаtiоп
in аiг (опе ion реr 10'5-1016 of nonionized molecules)
the particles аге believed to Ье imроrtапt climatological
agents with ргопочпсеd biological activity, including
therapeutic action. Biologically Ьепеfiсiаl and thегареu-
tic effects аге widely attributed to the negatively сhагgеd
ions (Tchijevsky 1960; Sulman et al. 1978 ; Кгоliпg
1985). Although пumеrоus ехреrimепtаl observations
оп аiг ion activities have Ьееп rерогtеd, little is kпоwп
about the ргimаrу mechanisms of the iпtеrасtiоп оf the
particles with biological objects-
lt is noticeable, that chemically described as О, and
recognised as а рагtiсlе геsропsiЬlе Гоr biological activity
оf negative аir ions (Кгuеgег and Reed 1976; Dolezalek
1985), is попе other than superoxide апiоп-гаdiсаl Oj .
The analysis оf physical ргосеssеs оf ргоduсtiоп ог аiг
ions in а соrопа disсhагgе (Goldstein 1982) indicated
а high probability оГ superoxide апiоп-гаdiсаl gепега-
tion. Моrеочеr mапу оГ the known physiological effects
оГ small negatively сhагgеd аir ions сап also Ье аttгiЬ-
uted to superoxide participation (reviewed Ьу Goldstein
1988). tn the ргеsепt study, we have evaluated the possi-
bility оf sчрегохidе production in aqueous media as а
геsult оГ the iпtеrасtiоп оГ both oxygen and пitrоgеп
ionization products at а gas/water interface. The оссuг-
rепсе оf Геаturеs сhаrасtеristiс оГ О, , rеасtiопs uпdег
these conditions mау Ье used to substantiate the hypoth-
esis оf the involvcment оf suрегохidе radicals оГ exoge-
поus огigiп in cell metabolism.
Materials апd methods
Reageпls. Fсггiсуtосhгоmе с was obtained Ггоm Воеhгiпgеr (USA)-
catalase and bovine Cu,Zn-suproxide dismutase (SOD) Гrоm Sig-
ma Chcmical Со. (USA). пitrоЬluе tеtгаzоlium (N ВТ) fгоm Reanal
(Нчпgаrу) апd tеtгапitгоmеthапе Ггоm Aldrich (USA). Luminol
оЫаiпеd Гrоm Yегечап Chemical Reagent Fасtогу (USSR) was
recrystallized twice Гrоm hуdrосhlогiс acid. The other rеаgепts used
wеге оГ rеаgепt gгаdе. Wаtеr was tгiрlу distilled in glass.
Gascs. Nitгоgеп was purified fгоm охуgеп Ьу fiItering thrоugh
saturated pyгogallol solution. Medical охуgеп and пitrоgеп mоп-
oxide апd аrgоп wеге used withou( Гuгthеr purification-
Еquiрlпепt. The аЬsогрtiоп sресtrа wеrс гесоrdеd using ап М-40
sресtrорhоtоmеtег (Саrl Zeiss, Jena. IrRG). Chemilumincscence
пеаsurеmепts wеrе рсrгогmеd with а selг-nlade сhеmilчmiпоmеtеr
equipped with а рhоtоеlесtrоп multiplier PhEU-l48 (Melz. Mos-
cow), as described Ь} Goldstein (1986). А special injection cell
made оГ ТеПоп was designed fоr gепсrаtiоп оГ negatively сhаrgеd
ions (Fig. l). Oxygen excitalion was регГогmеd iп а gas strеаm
Оffрriпt requesls ro., N.I. Goldstein
a

{lowing thrоugh а hollow рlаtiпum needle uпdеr llegativc voltagc
iп the rапgе of 2.5-6.0 kV frоm а stabilized sоurсе- Gas cxcitation
products gепегаtеd in the closed сhаmЬеr оГ 2 cm3 wсгс injectcd
bither onto the sчгfасе оГthе investigated solution iп arrother 2 сmЗ
сhаmЬеr, ог onto the sчrГасс оГа mrtliрогс filtеr (Vlаdiроr, USSR)
moistcned Ьу the test solution. Тhе elcctric сirсuit was саrthсd
via а platinurT arrodc with а surГасс o1- 5 mпr2. Thc tсmрсrаtuгс
ol-the solution was 20 t l" С; thc solulion was stirrсd Ьу а пrаgпсtiс
Stirrсr.
llпоlпеtrу. Negative аir ions wеrе generated iп а согопа dischaгge
uпdеr described conditions. Measurements ог аiг iorr сопсспtга-
tions wегс реrГоrmеd using the аsрirаtiоп сопdепsсr method with
ап аir ion сочпtег SAI-TGU-66m (Таrtu, Esthonia)- Uпdеr а псе-
dle potential оГ -3 kV, the conditional concentration оГ small
аir ions at а distance оГ l0 cm Гrоm thc needle was l06/cm].
L'еrriсуlосhrоmе с rеduсliоп. Reduction ог Геrгiсуtосhrоmе с was
dctermined in 0.1 М potassium phosphate ЬчГГеr, рН 7-1J, contain-
ing 10-а М EDTA, as described Ьу Fгidочiсh (1987а, Ь). The
initial cytochrome с сопсепtrаtiоп was 300 рМ.
Nitroblue telrazoliu!п rеduсtiоп. This was measured in 0.05 М ро-
tassium phosphate ЬuГfеr, рН 7.8, in the рrсsепсе оГ l0-4 М
EDTA and 500 пМ NBT ассоrdiпg to Апсlаir апd Voisin (l987).
Ехрегimепts showed that produced Гоrmаzап was quantitatively
аЬsогЬеd Ьу the Vladipor filtеr. АГtеr being dried in аiг. the filter
with the pгecipitate was dissolved in distilled руridiпе and the opti-
cal density оf the solution was rеаd at 560 пm veгsus руridiпе
solution containing а dissolved clear filtеr оГ the same size. This
рrосеdчrе avoided апу difficulties геlаtеd to the low solubilily of
гоrmаzап iп wаtеr.
НrО, assay. The assay Гоr the generation оГ НrО, was регfогmеd
with modiГrcations ассогdiпg to the method described Ьу Babko
et al. (1966). The геаgепt contained а mixture оГ0.1 М potassium-
phosphate-NaOН adjusted to рН 8.0, 500 рМ lчmiпоl and 50 цМ
[Со(NНз)п(NОr)r]Сl as а catalyst. Тhе reagent (1.8 ml) was гарid-
ly mixed with the solution fоr testing (0.2 ml) апd mеаsчгеmепts
of integгated chemiluminescence wеrе made dчriпg the Гrгst 10 s.
Uпdеr these conditions the liпеаr dерпdепсе оf chemilumines-
сепсе оп the hydrogen ргохidе concentration was found to Ье
in the гапgе оГ 120-500 пМ.
Results
Опе of the Йdеsрrеаd methods fоr аir ion gепеrаtiоп
is excitation in а silent соrопа dischaгge. The injection
се1[ shown in Fig. 1 was used to investigate supeгoxide
fоrmаtiоп both in охуgеп and uпdег iпtеrасtiоп оf the
пitгоgеп excitation products with water. The cell is ап
implementation of the model with а semi-infinite wirе
section previously considered Ьу Goldstein (1988). The
чirtuе оf this аррrоасh is the possibility to rерrоduсе
the main events оссurriпg in the interaction оГаir ioniza-
tion ргоdчсts Йth biological substrates. In огdеr to se-
lect optimal conditions fог thе operation оf the cell, сuг-
rепt чеrsus voltage dependences wеrе determined uпdеr
different rаtеs оГ nitrogen ог охуgеп flow (Fig. 2). The
results obtained гечеаlеd quite difIerent relationships Ье-
tween the счrrепt and gas flow rаtеs uпdеr conditions
of пitгоgеп and охуgеп ionization. Furthегmоге, higher
quantities оГсhагgе саrriеrs wеге ргоduсеd uпdег condi-
tions of nitrogen соmрагеd to охуgеп ionization.
Ozone gепеrаtiоп is possible during соrопа discharge
Гrоm а needle еlесtrоdе in the ргеsепсе оf охуgеп. Al-
Fig. l. Construction o!'injcction ceIl. 1, needle еIссtгt>dе; 2, high-
voIlagc sоUгсс;З. gas (О, ог N.) input;4, uррег рагt оГ iпjесtiоп
ccl1.5. holc lЪr gas output;6. space Гоr gas ionizirtion;7, пееdlс
Гсlг пеutrаl gas (N, ог Дr) iпрut:8, Vladipor llltсг; 9. body оГ
irljection cell; l0. space Гоr solution: 11, needle Гоr obtainirrg sam-
ples; 't 2. magnetic sliггег; 1_3. anode; l4. theгmostatc.jacket; 15.
iпstгumеп1 Гог nrcasuгirrg сlесtгiс сuгrепt
though the рагtiсlе does not show ргореrtiеs сhагасtеris-
tic fоr sцрегохidе and does not rеduсе fеrгiсуtосhrоmе
с and NBT, its oxidizing паtчге can iпfluепсе the rеsults.
Ноwечеr, it was found that uпdеr а negative voltage
of the согопа electrode оГ - з.0 + 0.1 kV, the ozone level
did not exceed погmаl values fоr ambient gas (арргох.
0.03-О.05 ppm).
Analysis оГ NBT rеduсtiоп showed that in ionized
oxygen medium at 0.1 рМ and gas flow rаtе оf 100 ml/
miп fогmаzап pгoduction waý liпеаг очеr at least 10 min
and the rеdцсtiоп was inhibited Ьу catalytic quantities
оГ superoxide dismutase (Fig. 3). The inhibition Ьу SOD
strопglу indicates the ргеsепсе оf Оr, in the аquеоus
medium. Superoxide Гоrmаtiоп in this case оссurs as
а геsult оГ mоlесчlаr охуgеп dissociation with the сар-
tuге of the еlесtrоп Ьу а пеutrаl охуgеп mоlесulе, as
Гоllоws:
О, +е- *о;, (1)
While diffusing into the solution, superoxide rеduсеs
NBT оп the iпtеrГасе between the gas and wаtеr phases.
As thеrе аrе по significant differences between the епег-
gies оГ охуgеп and пitгоgеп ionization (1315 and
1400 kJ/mol respectively), the Гollowing очегаll рrосеss
is possible iп аiг:
Nr-Nu* *е- (2)
119

]о.з
I
] о.2
I
250
20о -
,l 5о l
(чА)
з
High voltage (-kV)
Fig. З. Тiпе-соr:rsс оГ "',lý'H"i",r^zoliurn (NBT) геduсtiоп Ьу
negatir,cly iorrized oxygeIr: without additions (п п. 1). in the
ргеSеllсе оГ0.1 рМ, SoD (+ ,|.2) arrd wilh thcгmoinactivated
SoD (* *. ])
t (рА)
- 2.5
,- 2
Ф
,А l.B
]
I
\F-ig. 2. Vоltаmрсгiс сhагасtсгistiсs
,\I ll)c lI).i(,( lt,)tt t,t,ll :lч :r litncti,rn
tll- gas lltlrv rlrte, lollization оГ rri-
tг()gсl] (сuг\,сS .1 1 : .r,_0 2_50 цд)
апс1 oxvgelr (сurчсs 5 8:.t,-0
].5 tlA) ltrc ,чht)lчп at flow rаtсs
оГ _50. 'l00. 250 and 500 mltrпiп
гсsрссtiчсIу. 1tt.t,c,r1 : Depenclcnce
rlГ сttrrспt crtl l-titгоссп (сrrгr,с 1)
ltnd oxygctl (сuгчс 2) llow rlttcs
а1 clcctrtlclc potcrltia| _ -] kV
10о
Тhеrе is the possibility of а hydrated еlесtrоп е* fоrmа-
tion in the injection cell as а геsцlt оГ injection оГ nitro-
gen products into the solution. This еlесtrоп is capable
оГ both reduction оГ соmрlех molecules (for ехаmрlе
NBT), and оf forming Оr, in water. NBT reduction
observed during nitrogen ionization uпdег а сurrепt of
160 рА and gas flow гаtе оf 500 ml/min mау Ье due
to Оr, рrоduсtiоп mediated Ьу е"о. Consideгing that
е- hЪs а half-life оГ са. 2З0 ps in пеutгаl medium
(Sirеffеr l969). the supposed participation of the parti-
cles in the processes described above was evaluated indi-
Fig. 4. Fоrmаzап ассumulаtiоп on Vlаdiрог fiItегs causcd Ьу: Expt.
1. negativcly ionizcd nitгogen: Expt. 2. аГtеr addition оГ N.Ol
and Expt. 3. addition оГ ntlrrionized Nz (J)
rесtlу using the following reaction between е* and NrO
(Seki et al. 1976):
N,о+";.Л&ш,+ он+,оН (3)
It was assumed that nitrogen monoxide would inhibit
NBT rеduСtiоп caused Ьу both е* and Оr " Indeed,
simultaneous injection оf пitrоgеп mbnoxide and excited
nitrogen o.rto ih. SurГасе оf the filtеr inhibited NBT
rеduсtiоп. Analogous injection of аrgоп оr nonionized
nitrogen (instead оf NrO) did поt alter the overall quan-
tity Jf ГоrmаzаП ргоýuсtiоп, although the раttеrп оГ
Reducod NBT (чМ)
120
r5ог .a
i\
oL-
о ]оо 2оо эоо
l lu^)
-.-о5
+\'
]о
5оо
- 0.5
aФ
о

о б 10. 1б 2о 26
rkпо (mlп)
Iiig. 5. 'I'iпrе-соuгsс tlI'lЪrгiсуtосhrсlпlс t, гcclLtctitllt Ь1, rlcgativcly
ionizcd oxygctr rvithout SOD (r r. 1) апсi itl tltc 1-1tcsctlcc ol'
t pM SOD (+ _r ,2)
о Lo ,,й,п' 7-6 'o
Fig. 6. Тimе-соuгsе of H2O2 ,accumulation iп solution caused Ьу
negatively ionized охуgеп (l-r, 1) and in рrеsепсе оГ 30 пМ
SOD (1-1,2), 1рМ catalase (х-х, З) оr l рМ tеtгапitrо-
methane (в-о, 4)
the product distribution очеr the surfасе оГ the filter
was altered (Fig. а). This рhепоmепоп рrоЬаЬlу оссurs
due to сhапgеs in gas flow focusing. Taking into account
the fact that NBT reduction оп the surгасе оf the filtеr
was inhibited Ьу SOD (Fig. З) the presented геасtiоп
scheme mау Ье quite possible. Thus, we demonstгated
the possibility оf superoxide Гоrmаtiоп during the iпtеr-
action оf the ionization products of the principal atmo-
sрhегiс gases with water.
The evidence оГ О, , fоrmаtiоп in соrопа discharge
in oxygen was obtained while investigating fегriсуtосh-
rоmе с reduction and hydrogen peroxide Гогmаtiоп. Ас-
cumulation of these products was studied diгесtlу in so-
lution without а millipore filtеr. Quantitative compensa-
tion оГ the loss of solution due to the ечароrаtiоп and
rесочеrу of а рrimагу mass in these ехрегimепts was
achieved Ьу adding wаtег. As can Ье seen Гrоm the data
рrеsепtеd iп Fig. 5, oxygen ionization ргоduсts геduсеd
Гегriсуtосhrоmе с and this process was also inhibited
Ьу SOD. In рrоtоп-сопtаiпiпg media, supeгoxide is
known to uпdеrgо spontaneous dismutation, ассоmра-
nied Ьу hуdгоgеп регохidе fоrmаtiоп as а stable ргоduсt
(see Fгidочiсh 1983):
1]l
2о; + ?Il*-H2O2-1-(Jr (,1)
ThLrs. hусlгсlgсп регохidс ргоduсtiсlп coulcl aIso ргочiсiс
cvidcncc о Г sr_rperoxidc Го гпlа t ion, LJsi п g l rrrn i rT tll-dcpcrl -
dспt cherllilttIl,tittcsc:cncc. lt ri,irs loLrncl that tlcgittivc tlxr -
gcrl iortizalitln irlclttcecl I I.(). pгtlcltictiol1 il1 aIr irlitilrl
гаtс оl'са. _50 ц1\4 Itllin агiсl this valirc ц,аs incrcitscci ccrtt-
sidегаЬlу Lrpclrl aciditiot-t о1- ]0 riM SOD. z\dclititln tll-
tIlc stlрсгохidс sсачеtlgсг iеtгаrlitгоrllсthапс ог catitlltsc
into thc systclll r.vithoLrt SOD complctely pгcvcr-rted thc
accurrlulaticln tlГ hydгogeri рсгttхiсlе 1Fig. 6).
'I'he геstrlts obtained Il1ay sсгче as evidcrTcc thаt а
ргоduсt lravirrg the пlаiп ргорегtiеs оГ suрегохiсlе is
Гоrпlеd lts а геsult оГ оху_ееп and пitгоgсп iotrizetltlt-l
itl согопа dischargc. (]aIculaticlrls рсгtilгrlrсd tЬг Nt]-Г
геduсtiоп апd lrусiгоgеп регохiсlе ргtlduсtitlll shorvcd
that thе stcady-state гаtе оГ gепсгаtiо11 оГ the ргосluсt,
which we idепtiГу as О, . is са. 1-5 2 0 х 10 б Mi Illirl.
Discussion
Uпdег паtuгаl conditions оГ аtmоsрhегiс аir iorrizlttitln,
superoxide ргоduсtiсrп mау 1ake place both due to diгect
oxygen iorrization and as гestrlt оГ пitгоgеtr iorrization
duгiпg the iпtеrасtiоп оГ ionized pгoducts r,",ith oxygen-
corrtaining aqucous media. Fгее еlесtгопs ц,hiclr аррсаr
at the еагlу stirges оГ gas ionization mау have diГГегепt
епегgiеs. IГ the еlесtrоп епегgу cxcccds 360 kJ/nrol, the
following rсасtiопs аrс assumed to take place, liссогdiпg
to Pethig (l984):
е- *Or--+QlQ-
Оr*О-*О+оr,
Superoxide fогmаtiоп was also shown to Ье рrоЬаЬlе
via iпtеrасtiоп оf ionized gases with wаtег in the Гоllоw-
ing геасtiопs:
^_ Нrо ,с
L ----+ -aq
Оr+е;-о;
The scheme shown in Fig. 7 postulates sечегаl pathways
оf Or,generation in gaseous medium and at ап аir/wаtег
iпtеrГасе. The limited lifetime оГ suрегохidе in aqueous
mеdium ргечепts the diГГusiоп оГ this product. Due to
this fact its biological activity сап manifest itselГ опlу
at the Ьоuпdаrу surГасе. These fеаturеs ргоЬаЬlу explain
the well-known obseгvations (see гечiеw оf Кruеgег and
Reed 1976) that аiг ions have stгопgег, mоге lethal еГ-
fects upon miсгооrgапisms оп the surfасе оГ а liquiq
сulturе соmрагеd to those cells iп dеерег lауегs. The
observations оГ Kellog et al. (1979; see also Rosenthal
and Веп-Нur 1980) оf the ргоtесtiче еГГесt оГ SOD оп
Staphylococcus albus trеаtеd with negative аir ions may
Ье attгibuted to the elimination оГ suрегохidе.
Iп contrast to superoxide gепеrаtеd Ьу гadiolysis оr
in the ргосеssеs оГ cell metabolism, the liГetime оf аiг
ions iп а gaseous mеdium mау rеасh dozens оГ seconds.
The disappeaгance оГ negative ions uпdег these condi-
tions is caused evidently not only Ьу ion гесоmЬiпаtiоп
iп the gas phase, but also Ьу О, , dismutation iп the
рrеsепсе оГ wаtег чароuг. This mау explain а well-
(5)
(6)
(7)
(8)
Нуdrорэrохld (uМ)

|72
l'ig. 7. [)roposcd gепегаl schcme Гоr supeгoxide Гormlttiotl ill цltч-
cous and ill aqueous phases as а rеsult оГ охуgеп and пttгоgеrt
ncgative iclnization
known iпfluепсе of аiг humidity on the physiological
еfГесts оГ negative аiг ions, as described Ьу Tchijevsky
(1960), Кгuеgег and Reed (1976) and others.
The results obtained in this study sчррогt suggestions
оГ Ктuеgеr et al. (1975) апd Кruеgег and Reed (1976)
оп the рrоЬаЬlе participation оf frее radicals in the bio-
togical activity of аir ions. It must Ье emphasized that
the biological effects of negative ions аrе not related
solely to superoxide, Ьut also to hуdгоgеп peroxide, hy-
drохуl radicals and оthеr activated охуgеп species (fоr
rечiеw see Byczkowski and Gеssпег 1988; Fridovich
1989).
Thus, the biological activity of negative аir ions can
Ье conditioned Ьу sечегаl active products and, evidently,
аrе ргimаrilу due to the superoxide anion. Keeping in
mind that negative аir ions аrе an integral component
оf епчirопmепt. А ргоmiпепt ecological and evolution-
агу rоlе of exogenous superoxide is suggested. Опе сап
also рrороsе that the biological effects of the radical
must depend оп the level оГ organization оГ living mat-
tег: while miсrооrgапisms and miсrоsсорiс fungi аге
killed оr lose thеiг viability, the interaction оf this ехоgе-
поus superoxide with tissue rесерtоrs of mammals (mu-
cous mеmЬгапе оf the поsе and the аiгwауs, skin, etc.)
арраrепtlу sеrчеs as а basis fог regulation оf чагiоus
physiological Гuпсtiопs. Thus thеге mау exist sечегаl
mechanisms оГ tоlеrапсе towards this fасtоr. The possi-
ble гоlе оГехоgепоus Оr- as an adaptogen tоwагds the
с1-1ссt<lгs tlt' thc agcnts tl-rat irldircc thсiг clamagirrg сt-Гссts
r,ilt 1-1:tгtic:lpatiorl ol- ltctir atcd охуgс11 spccics is srrg-
geS le(l .
llеtсrепсеs
,\rtсl:riг ('. \ilrsrll Il (l9t7) Nlll0blrlc tclг1l/OllLll]-] гctittctitlIl, Ill:
( iгссtlrr tticl ltA (cd ) ('l{(' hlrrrclbtirlk tll' tllcthtltls lЪг ох1,_чсп
гаdiсаl гсsс:tгсh CIt(] l)t css. []tlcll I{аttlп. }'ltlгidil. рр l2_] 1З2
l]abkrl АК. Г)uЫlrсllkrr [-I. [-uktlvsklrr,:r NN1 (l96(l) ('hсrпiluпriп-
cscctlt aTrirlysls, Natrktlra [)Lrrrika Kicv (in Rtrssiarl)
l]_yczkouski _l1-. (]csslrcг l' { 19t{ti) tJiological гtlIс rll' supcrclxidc
itlrl гасliсаl. Iпt J I}itrchcrll ]0:5(l9 58()
[)tllczlrlck ll (I9S5) Ilспl:iгks rlп thc phrsics оl'аtпltlsрhсгiс iorrs
(tl:ttut;tl atlci:rгtlliclai) ltlt .I []irlrrlctctlltll f9:]l 1 22l
[:гitillyiсh I (l98]) Sullcгtltirlc гаt]iсitl: all clldO!]cll()[l\ tO\icilltt,
Atltlu Rcr, [)lrltгtlractll Tclxictrl ]]:2l() 257
Ггidочiсh I (l987a) ('lttlcltгtltltc ('. Iп: (lгccrlrvaltl RA (cd) CRC
harldbook tll'tncthtlds iilr tlxvgcrt rаdiсаl rсsеагсh. CIl(] I)геss.
Brlca Rirton. I,Iоriсlа. рр l 2l 1 22
I-гititlvich I {l91{7b) (-чtсlсhrtlпlс (', Irl: (iгcctrlvalcl ItA (cci) CRC
handbtltlk о[' пlсthtlds lilr охуgсгl radical rсsсагсh. (]RL] Ргеss,
[]rlc:a Rattltl. []loгidir. рр 21 _] 2l 5
I'гirlочiсh I ( l9lt9)SLrpcroxide disnrulascs Ап adaptatitln to ] pat,a-
Trllrgtlctic gas .l liiol Сhспr ]{i:1:]16lr ] ,161
Gоlсjstсiп N I ( l9S]) 'I'hc stability ol' 5опlс ЬiоSuЬStгаtсs and its
пltldсls tcl ;-lcгoxidatitlri iп аtпrоsрl-tсгс tlГ аiг itltls. lп: [Jluger
А (cd) t-lr,сг ссllLrlаг апd sLtbcclluiar pathclltlgy_ Zilllitnc. Riga.
рр 91 96 (rп RLlssi;rlr)
(lolrlstcirr N I ( l986) ChcTlrluпlillcsccIlt illdicat()l, Iri : Jurачlсw А
(ccl) []iolumrrlcsccncc iп аgгiсr.rltuгс, Ail LJnitln State Agricul-
tuгtrl Ac:rclcmr Моsсош,. рр 27 28 (iп Russian)
Gtlldstein Nl (1988) Аiг ions:Thc p,-lssible гоlс оГасtiчаtеd oxygcn
spccies iп пrссhапisms оГ biological action. Itt: Goidstein NI
(cd) Охi,gсп гadicals in сhеmistгу, biology апd medicine. Riga
Medical Institutc. рр 80 108 (in Russian)
Kcllog EW. Yosr tr4(i. Вагllrirkur N. Кгuсgсг АР (1979) Suреrох-
icle involvcrrrcrrt in thc bacteгrcidial еllъсt ог negative аiг ions
оп Slrr2llг/oсrrсr,tr,r rrlbll,r. Naturе 2[l1:400 40l
Кгбliпg Р (l985) Natural and аrtiПсаllу ргоduсеd аir ions а
biologically rсlсчапt climate Гасtоr'] [пt J Вiопеtеогоl 29:23З
212
Кгuеgсг АР, Reed EJ (1976) Biological impact оГ small аir ions.
Scicncc 19]: l209-1213
Кгuеgег АР. Reed EJ, l]гооk Kt}. Day мв (l975) Аiг ion action
оп Ьасtсгiа, Int J Вrоmеtсогоl l9:65 7l
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аiг ions: Rclcvancc to biological studies- Methods Enzymol
105:2З8 248
Rosenthal l. Веп-I]ur Е (l980) Superoxide iпчоIчегпспt iп negativc
air iоп effects. Nature 288 (597?):7]9
Seki Н, tlan YA. Ilan Y, Stein G (1976) Reactions оГ the Геrгi/
Геггсlсуtосlrrоmе-С system with suрсгохidс/охуgеп and СО, /
СО, studicd Ьу list pulse гаdiоlуsis. Biochcm Bioplrys Acta
440: 57_]-586
StrеГГег с (1969) Stгahlcn-Biochcmie. Sргiпgеr, Веrliп I{cidelberg
New Yогk, р 195
Sulman FG, Levy Г), [-uпkап L. РГеuГег Y, TaI Е (1978) Absencc
оГ hагmГul еГГесts оГ ргоtrасtеd negative аir ionization. lnt J
Вiоmеtеогоl 22;5]-58
TchijevskY AL (1960) Аеrоiопifiсаtiоп in national есопоmу, Pulэ-
lishing House ог the state Рlапiпg commision ог the ussR,
Moscow. р 758 (iп Russian)
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