Upload
kaychi-z
View
222
Download
0
Embed Size (px)
Citation preview
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
1/10
1975, 30(2):229.Appl. Microbiol.
MelnickCharles P. Gerba, Craig Wallis and Joseph L. Organisms
Production and the Fate of ResidualHousehold Toilets: DropletMicrobiological Hazards of
http://aem.asm.org/content/30/2/229Updated information and services can be found at:
These include:
CONTENT ALERTS
more»new articles cite this article),Receive: RSS Feeds, eTOCs, free email alerts (when
http://journals.asm.org/site/misc/reprints.xhtmlInformation about commercial reprint orders:http://journals.asm.org/site/subscriptions/To subscribe to to another ASM Journal go to:
on S e p t em b er 1 0 ,2 0 1 3 b y g u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/cgi/alertshttp://aem.asm.org/cgi/alertshttp://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/cgi/alerts
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
2/10
Appun
M I C R O B I O L O G Y , A u g . 1 9 7 5 ,
p .
2 2 9 - 2 3 7
C o p y r i g h t 0
1 9 7 5 A m e r i c a n
S o c i e t y
f o r
M i c r o b i o l o g y
V o l .
3 0 ,
N o . 2
P r i n t e d
i n
U . S . A .
M i c r o b i o l o g i c a l
H a z a r d s
o f H o u s e h o l d T o i l e t s :
D r o p l e t
P r o d u c t i o n
a n d
t h e F a t e
o f
R e s i d u a l
O r g a n i s m s
CHARLES
P . G ERB A, C RA IG
WALLIS,
AND JOSEPH
L .
MELNICK*
D e p a r t m e n t
o f
V i r o l o g y
a n d E p i d e m i o l o g y ,
B a y l o r
C o l l e g e o f
M e d i c i n e ,
H o u s t o n ,
T e x a s
7 7 0 2 5
R e c e i v e d f o r p u b l i c a t i o n
1 2 March
1 9 7 5
L a r g e
n u m b e r s
o f b a c t e r i a
a n d v i r u s e s
w h e n
s e e d e d
i n t o h o u s e h o l d t o i l e t s
were
s h o w n t o
r e m a i n i n
t h e b o w l
a f t e r
f l u s h i n g ,
a n d even c o n t i n u a l
f l u s h i n g
c o u l d
n o t
remove
a
p e r s i s t e n t
f r a c t i o n . T h i s was
f o u n d t o
b e
d u e t o
t h e
a d s o r p t i o n
o f
t h e
o r g a n i s m s
t o
t h e
p o r c e l a i n
s u r f a c e s
o f
t h e
b o w l ,
w i t h
g r a d u a l
e l u t i o n
o c c u r r i n g
a f t e r
e a c h
f l u s h .
D r o p l e t s p r o d u c e d
b y f l u s h i n g
t o i l e t s were
f o u n d t o
h a r b o r b o t h
b a c t e r i a a n d
v i r u s e s
w h i c h h a d b e e n
s e e d e d .
The
d e t e c t i o n o f
b a c t e r i a
a n d
v i r u s e s
f a l l i n g o u t o n t o
s u r f a c e s
i n
b a t h r o o m s
a f t e r
f l u s h i n g
i n d i c a t e d
t h a t
t h e y
r e m a i n a i r b o r n e
l o n g
e n o u g h
t o
s e t t l e
on
s u r f a c e s
t h r o u g h o u t
t h e
b a t h r o o m .
T h u s ,
t h e r e
i s a
p o s s i b i l i t y
t h a t a
person
may a c q u i r e
an
i n f e c t i o n
f r o m
an
a e r o s o l
p r o d u c e d
b y
a
t o i l e t .
T h e
t r a n s m i s s i o n
o f d i s e a s e
b y
a e r o s o l s f r o m
t o i l e t s
h a s
r e c e i v e d
o n l y
l i m i t e d
s t u d y .
I t
h a s
b e e n
s u g g e s t e d
t h a t ,
a s i d e f r o m
c o u g h i n g
a n d
s n e e z i n g ,
t h i s m u s t
b e
t h e
m o s t
common
p r o -
c e s s
i n v o l v e d i n t h e
g e n e r a t i o n
o f
i n f e c t i o u s
a e r o s o l s
( 6 ) .
D a r l o w a n d B a l e
( 6 ) d e m o n s t r a t e d
t h e
p r o d u c t i o n
o f
b a c t e r i a l
a e r o s o l s ,
w i t h
t h e
a i d o f b o t h
a
l i q u i d
i m p i n g e r
a n d
a
s l i t
s a m p l e r ,
f r o m
f l u s h e d b o w l s
c o n t a i n i n g S e r r a t i a
m a r c e s c e n s .
T h e s e a e r o s o l s w e r e
f o u n d t o
p e r -
s i s t
f o r
a t
l e a s t
1 2
m i n
a f t e r t h e
f l u s h .
The
g e n e r a t i o n
o f a e r o s o l s
b y
t o i l e t s
s e e d e d w i t h
c o l i f o r m b a c t e r i a
h a s
b e e n
d e m o n s t r a t e d
b y
B o u n d a n d
A t k i n s o n
( 3 )
a n d
m o r e
r e c e n t l y b y
Newsom
( 1 4 ) .
T h e
s i z e o f
p a r t i c l e s p r o d u c e d
b y
t h e
f l u s h i n g
t o i l e t w a s
f o u n d
t o
b e
i n t h e
r a n g e
t h a t
w a s
c a p a b l e
o f
r e a c h i n g
t h e
l o w e r
r e s p i r a -
t o r y
t r a c t ( 6 ) .
I n
a d d i t i o n ,
p a t h o g e n i c
f e c a l
c o n t a m i n a n t s ,
s u c h
a s E s c h e r i c h i a
a n d S a l -
m o n e l l a , h a v e
b e e n
i s o l a t e d
f r o m
t h e
r e s p i r a -
t o r y
t r a c t
o f
i n f e c t e d h u m a n s
( 6 ) .
T h e f a l l o u t o f
d r o p l e t s
c o n t a i n i n g
p a t h o g e n s
o n
b a t h r o o m
s u r f a c e s
i s
a l s o o f
c o n c e r n ,
s i n c e
h a n d
c o n t a c t w i t h
c o n t a m i n a t e d
s u r f a c e s
c a n
r e s u l t
i n
s e l f - i n o c u l a t i o n
b y
t o u c h i n g
o f
t h e n o s e
o r m o u t h
( 1 1 ) .
H u t c h i n s o n
( 1 2 )
t r a c e d t h e
s p r e a d
o f
S h i g e l l a
s o n n e i
i n
a
n u r s e r y
s c h o o l
t o
c o n t a m i n a t e d
t o i l e t
s u r f a c e s . C o n t a c t
w i t h
c o n -
t a m i n a t e d
s u r f a c e s h a s a l s o
b e e n s h o w n t o
b e
i m p o r t a n t
i n
t h e
s p r e a d o f
a n i m a l
v i r u s e s
( 1 1 ) .
To
d a t e
n o
i n f o r m a t i o n
e x i s t s o n t h e
g e n e r a -
t i o n o f v i r a l
a e r o s o l s
b y
h o u s e h o l d t o i l e t s .
T h i s
s t u d y
w a s
c a r r i e d
o u t
t o
g a t h e r m o r e i n f o r m a -
t i o n
o n
t h e
f a t e o f b o t h
b a c t e r i a a n d
v i r u s e s
i n
f l u s h e d
t o i l e t s .
MATERIALS
AND
METHODS
V i r u s e s
a n d
v i r u s
a s s a y s .
E . c o l i
b a c t e r i o p h a g e
MS-2
a n d a
p l a q u e - p u r i f i e d
l i n e
o f
t y p e
1
p o l i o v i r u s
( s t r a i n
L S c ) w e r e u s e d
i n t h i s
s t u d y . M S - 2 ,
l i k e
p o l i o v i r u s , i s
a
s m a l l ( 2 5 - n m
d i a m e t e r )
i c o s a h e d r a l
r i b o n u c l e i c
a c i d
v i r u s . A l l
b a c t e r i o p h a g e a s s a y s w e r e
d o n e
b y
a m o d i f i c a t i o n
o f
t h e
a g a r
o v e r l a y m e t h o d a s
d e s c r i b e d
b y
Adams
( 1 ) . O v e r l a y a g a r a n d
b r o t h u s e d
f o r
b a c t e r i o p h a g e
s a m p l e s
w e r e
p r e p a r e d
a c c o r d i n g
t o
D a v i s
a n d
S i n s h e i m e r ( 8 ) .
S t o c k
p o l i o v i r u s w a s g r o w n
i n
b a b o o n
k i d n e y
c e l l s ,
c o n c e n t r a t e d
1 0 - f o l d , a n d
p a r t i a l l y
p u r i f i e d
b y
m e m b r a n e
c h r o m a t o g r a p h y
( 2 2 ) .
P o l i o v i r u s
s a m p l e s
w e r e
d i l u t e d
i n
t r i s ( h y d r o x y -
m e t h y l ) a m i n o m e t h a n e - b u f f e r e d
s a l i n e
c o n t a i n i n g
p e n i c i l l i n
( 1 0 0 U / m l )
a n d
s t r e p t o m y c i n
( 1 0 0
g g / m l ) .
P o l i o v i r u s
a s s a y s w e r e
m a d e
w i t h B S C - 1
c e l l s
b y
t h e
p l a q u e - f o r m i n g u n i t
m e t h o d a s
u s e d
i n
t h i s
l a b o r a t o r y
( 2 0 ) .
B a c t e r i a
a n d
b a c t e r i a l
a s s a y s . A s t r a i n
o f E . c o l i
i s o l a t e d f r o m
d o m e s t i c
s e w a g e
w a s u s e d ( i d e n t i f i c a -
t i o n
b a s e d o n
I m V i c
t e s t ) .
A l l
c o l i f o r m
a s s a y s w e r e
p e r f o r m e d o n
L e v i n e
e o s i n
m e t h y l e n e
b l u e
( E M B )
a g a r . T o t a l
a e r o b i c
b a c t e r i a l
c o u n t s w e r e
p e r f o r m e d
o n
S t a n d a r d
M e t h o d s a g a r ( B B L ,
C o c k e y s v i l l e , M d . ) .
C u l t u r e s
o f
E .
c o l i
u s e d i n
s e e d i n g e x p e r i m e n t s
w e r e
g r o w n
o v e r n i g h t
i n
T r y p t i c a s e s o y b r o t h
( T S B ) ( B B L ,
C o c k e y s v i l l e ,
M d . ) .
A l l
b a c t e r i a l
s a m p l e s
w e r e
d i l u t e d
i n
t r i s ( h y d r o x y m e t h y l ) a m i n o m e t h a n e - b u f f e r e d s a -
l i n e .
T o i l e t s .
S t a n d a r d
h o u s e h o l d t a n k o r
v a l v e
t o i l e t s
w e r e
u s e d . T h e t a n k
t o i l e t s h a d a r e s e r v o i r
c o n t a i n i n g
a p p r o x i m a t e l y
2 0
l i t e r s ,
o f
w h i c h
1 3 . 7 l i t e r s
w a s
r e l e a s e d
d u r i n g
a
f l u s h , u n l e s s
o t h e r w i s e n o t e d .
T h e
b o w l
o f t h e
t a n k - t y p e
t o i l e t
c o n t a i n e d
a
v o l u m e
o f 3 . 5
l i t e r s
u n l e s s
i n d i c a t e d o t h e r w i s e .
T h e
b o w l
v o l u m e o f
t h e
v a l v e
t o i l e t
w a s
a p p r o x i m a t e l y 4 . 2
l i t e r s ,
w i t h a
s t a n d a r d
b u t
u n d e t e r m i n e d
a m o u n t o f
w a t e r r e -
l e a s e d
d u r i n g
a
f l u s h . I n
t h e
v a l v e t o i l e t
u s e d , t h e
2 2 9
on S e p t em b er 1 0 ,2 0 1 3 b y g
u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
3/10
2 3 0 GERBA,
W A L L I S ,
A N D MELNICK
a m o u n t
o f
w a t e r r e l e a s e d w a s
d e p e n d e n t
o n t h e
w a t e r
l i n e
p r e s s u r e i n t h e b u i l d i n g ,
w h i c h
w a s
u s u a l l y
c o n s t a n t .
B e f o r e b e i n g
s e e d e d
w i t h b a c t e r i a
o r
v i r u s e s
t h e t o i l e t s w e r e
c l e a n e d
w i t h
c o m m e r c i a l l y
a v a i l a b l e
c h l o r i n e - c o n t a i n i n g c l e a n s e r
a n d f l u s h e d
r e p e a t e d l y
t o
e l i m i n a t e a n y
b a c t e r i a
o r
v i r u s e s
n a t u r a l l y
p r e s e n t .
A s o l u t i o n
o f 5
g
o f s o d i u m
t h i o s u l f a t e
p e r
l i t e r
w a s
t h e n
a d d e d
t o
i n a c t i v a t e
a n y
c h l o r i n e
p r e s e n t
i n
t h e
w a t e r , a t
a
r a t i o
o f
1 m l o f
s o l u t i o n
t o
1
l i t e r o f
t a p w a t e r . A t a n k - t y p e
t o i l e t
w a s u s e d
i n
a l l
e x p e r i -
m e n t s u n l e s s
i n d i c a t e d
o t h e r w i s e .
RESULTS
R e s i d u a l
i n f e c t i o u s
m a t e r i a l
i n
t o i l e t
b o w l s .
T h e
f i r s t
g r o u p
o f
e x p e r i m e n t s
w a s
c o n d u c t e d t o
d e t e r m i n e
t h e
f a t e
o f
i n f e c t i o u s
a g e n t s
i n
t o i l e t
w a t e r s a f t e r
f l u s h i n g
o f a
t y p i c a l
d o m e s t i c t o i l e t .
T o i l e t
b o w l s
w e r e f i r s t c l e a n e d
a s
d e s c r i b e d
i n
M a t e r i a l s
a n d M e t h o d s a n d
t h e n s e e d e d
w i t h
e i t h e r
a n
o v e r n i g h t
c u l t u r e
o f
E . c o l i o r
MS-2
p h a g e .
I n
b o t h
c a s e s t h e
o r g a n i s m s w e r e
s u s p e n d e d
i n
1 0 0
m l
o f
TSB
t o
s i m u l a t e t h e
p r e s e n c e
o f
o r g a n i c
m a t t e r f o u n d
i n
a c t u a l f e c a l
m a t e r i a l .
A f t e r
t h e
b o w l
w a t e r
w a s m i x e d , a b a s e l i n e s a m p l e
w a s
o b t a i n e d .
T h e
t o i l e t w a s
t h e n
f l u s h e d ,
a n d t h e t o i l e t
w a t e r
w a s
s a m p l e d
f o r r e s i d u a l
o r g a n i s m s .
T h i s
p r o c e -
d u r e w a s
r e p e a t e d
s e v e r a l
t i m e s ,
a n d
t h e r e s u l t s
o f
a
t y p i c a l e x p e r i m e n t
f o r b o t h b a c t e r i a
a n d
v i r u s e s c a n b e
s e e n
i n
F i g .
1 .
A s
a n t i c i p a t e d ,
t h e
i n i t i a l f l u s h e l i m i n a t e d
t h e
m a j o r
p r o p o r t i o n
o f
e x o g e n o u s l y a d d e d
o r g a n i s m s . H o w e v e r ,
a f t e r
r e p e a t e d
f l u s h e s ,
i n s t e a d o f
d i m i n i s h i n g ,
t h e r e
w a s o f t e n
a n
i n c r e a s e
i n t h e
n u m b e r
o f
r e s i d u a l
o r g a n i s m s
d e t e c t e d
i n
t h e
b o w l .
I n t h e
c a s e
o f
b o t h
b a c t e r i a
a n d
v i r u s e s ,
t h e
n u m b e r
o f
o r g a -
n i s m s
i n
t h e
b o w l r e a c h e d a
p l a t e a u
b e l o w
w h i c h
t h e i r
n u m b e r
c o u l d n o t b e
r e d u c e d ,
e v e n
a f t e r
r e p e a t e d
f l u s h i n g .
F r o m
t h i s
e v i d e n c e , i t
a p p e a r e d
t h a t
s i g n i f i c a n t n u m b e r s
o f
b a c t e r i a
a n d
v i r u s e s w e r e
b e i n g a d s o r b e d
t o
t h e
t o i l e t
p o r c e l a i n
a n d t h e n e l u t e d
d u r i n g
t h e
f l u s h i n g
a c t i o n .
T o t e s t t h i s
s p e c u l a t i o n ,
t h e
p r e v i o u s e x p e r i -
ment w a s
r e p e a t e d , a n d , a f t e r
t h e
t h i r d f l u s h ,
T w e e n
8 0 ,
a n o n i o n i c
d e t e r g e n t ,
w a s a d d e d
t o
y i e l d
a
f i n a l c o n c e n t r a t i o n
o f 0 . 1 i n
t h e b o w l
w a t e r .
T h e
s i d e s
o f
t h e
b o w l
w e r e
t h e n
s c r u b b e d
w i t h a
b r u s h , a n d a
s a m p l e w a s
o b t a i n e d
f o r
a s s a y .
T h e
r e s u l t s
o f
t h i s
e x p e r i m e n t f o r
E . c o l i
a r e s h o w n
i n
F i g .
2 . A
1 0 , 0 0 0 - f o l d
i n c r e a s e i n
t h e
b a c t e r i a l
c o u n t
o c c u r r e d a f t e r t h e
T w e e n
8 0
t r e a t m e n t , i n d i c a t i n g
t h a t
b a c t e r i a
w e r e
a d -
s o r b i n g
t o t h e
p o r c e l a i n
s u r f a c e s
a n d c o u l d
b e
e l u t e d
b y s c r u b b i n g
i n t h e
p r e s e n c e
o f a n
e l u e n t
s u c h
a s
T w e e n 8 0 . When
t h e t o i l e t w a s
f l u s h e d
a f t e r t h e T w e e n 8 0
t r e a t m e n t , a l m o s t
a l l
o f
t h e
b a c t e r i a
w e r e r e m o v e d f r o m
t h e
b o w l
w a t e r
A P P L .
M I C R O B I O L .
1 2
- J
I -
w
I - -
z
c r
w
- J
0
0
0
- J
1 1
1 0
9
8
7 -
6
5
4 -
3
0
0
i 2
3
4
5
6
7
NUMBER
OF FLUSHES
F I G .
1 . E f f e c t
o f
f l u s h i n g
o n
r e m o v a l
o f e x o g e -
n o u s l y a d d e d b a c t e r i a
a n d
v i r u s e s t o
t h e t o i l e t b o w l .
T h e
l o g , ,
n u m b e r o f o r g a n i s m s i n d i c a t e d a b o v e
w a s
a d d e d t o
t h e
t o i l e t b o w l
w a t e r , a n d
w a t e r
s a m p l e s
w e r e r e m o v e d f r o m t h e
b o w l
f o r a s s a y
a f t e r
e a c h f l u s h .
L o g , 1
v a l u e s
o f o r g a n i s m s r e p r e s e n t t h e
n u m b e r
p r e s e n t
i n
t h e e n t i r e v o l u m e c o n t a i n e d i n t h e
t o i l e t
b o w l .
S y m b o l s : 0 , MS-2 p h a g e ;
0
E .
c o l i .
( F i g .
2 ) .
I n o t h e r
e x p e r i m e n t s i t w a s f o u n d t h a t
s i m p l e m i x i n g
o f
T w e e n
8 0
i n t o
t h e
b o w l
w a t e r
o r
s c r u b b i n g t h e
b o w l
w i t h
a
b r u s h
w i t h o u t
a d d i t i o n o f Tween 8 0
w e r e
e q u a l l y e f f i c i e n t
i n
t h e r e m o v a l o f
b a c t e r i a f r o m t h e s i d e s o f
t h e
t o i l e t b o w l .
When t h e
same
e x p e r i m e n t
w a s
p e r f o r m e d
w i t h
p o l i o v i r u s o r
MS-2 p h a g e
( F i g .
3 ) ,
a n
i n c r e a s e
i n t h e n u m b e r
o f v i r u s e s
w a s
a l s o
n o t e d
a f t e r T w e e n
8 0
t r e a t m e n t ,
b u t
s u b s e q u e n t
f l u s h i n g r e s u l t e d
i n
o n l y a g r a d u a l
l o s s o f v i r u s
f r o m
t h e b o w l
w a t e r .
T h u s ,
i t
d i d
n o t a p p e a r
t h a t a l l
o f t h e
v i r u s e s w e r e e l u t e d
f r o m
t h e b o w l
s u r f a c e s
b y
t h e
Tween
8 0
t r e a t m e n t . P e r h a p s
v i r u s e s a r e
m o r e
d i f f i c u l t
t o
d e s o r b
f r o m
t h e
p o r o u s
s u r f a c e
o f t h e
p o r c e l a i n
t h a n
b a c t e r i a .
To
d e t e r m i n e t h e n u m b e r o f
b a c t e r i a u s u a l l y
p r e s e n t
i n
t o i l e t s ,
t o i l e t
b o w l s w e r e
m o n i t o r e d
i n
r e s t a u r a n t s ,
s e r v i c e
s t a t i o n s , e t c . T o i l e t s
w e r e
t r e a t e d w i t h Tween
8 0 a n d
a g i t a t e d
t o
e l u t e
b a c t e r i a f r o m
t h e b o w l
s u r f a c e s .
A
s a m p l e o f
b o w l
w a t e r
w a s t h e n
r e m o v e d a n d
p l a t e d
o n
b o t h EMB
a g a r a n d
T r y p t i c a s e s o y
a g a r .
T h e
r e s u l t s o f
t h e s e
e x p e r i m e n t s
a r e
s h o w n
i n
T a b l e
1 .
A e r o b i c
b a c t e r i a
w e r e p r e s e n t a t l e v e l s f r o m
on S e p t em b er 1 0 ,2 0 1 3 b y g
u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
4/10
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
5/10
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
6/10
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
7/10
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
8/10
MICROBIOLOGICAL
HAZARDS
OF HOUSEHOLD
TOILETS
2 3 5
T A B L E 9 .
Number
o f
MS-2
p h a g e
f a l l i n g
o u t
o n
b a t h r o o m
s u r f a c e s a f t e r
t o i l e t
f l u s h i n g
T o t a l
T o t a l n o .
o f PF U E s t i m a t e d
PFU a f t e r
n o . o f
PF U
T i m e
e l u t e d c o r r e c t i o n
o n
f l o o r
V e n t i -
a f t e r f r o m a l l f o r e f -
s u r f a c e
l a t i o n c
g a u z e
f i c i e n c y
a r e a o f
p a d s a
o f
b a t h r o o m
e l u t i o n '
0 - 2
4 , 1 0 7 5 , 1 7 5
3 5 , 4 6 8
C l o s e d
2 - 4
2 4 4
3 0 7 2 , 5 3 2
C l o s e d
4 - 6
0
0
0 C l o s e d
0 - 2
2 0 9
2 6 3
1 , 5 4 0
O p e n
2 - 4 0
0 0 O p e n
4 - 6
0 0
0
O p e n
' R e p r e s e n t s t h e
a v e r a g e o f f i v e
t o s i x e x p e r i m e n t s
f o r e a c h
2 - h
p e r i o d . I n e a c h , a p p r o x i m a t e l y 4
x 1 0
p l a q u e - f o r m i n g u n i t s
( P F U )
o f M S - 2
p h a g e w e r e
a d d e d t o t h e b o w l
b e f o r e f l u s h i n g . E l u a t e
f r o m
e i g h t
g a u z e
p a d s w a s
p o o l e d b e f o r e a s s a y .
T h e
l o c a t i o n
o f
t h e
g a u z e
p a d s
i n
t h e
b a t h r o o m
c a n
b e
s e e n
i n
F i g .
5 .
T h e
a v e r a g e
e f f i c i e n c y o f e l u t i o n w a s a p p r o x i -
m a t e l y
7 9 .
e
c
T h e
v e n t i l a t i o n
o f
t h e r o o m w a s c o n s i d e r e d
c l o s e d
w h e n a l l a i r v e n t s i n t h e
r o o m w e r e s e a l e d a n d t h e
b a t h r o o m d o o r r e m a i n e d
c l o s e d .
T A B L E 1 0 . D e t e c t i o n o f
n a t u r a l l y
o c c u r r i n g
c o l i f o r m s
o n
b a t h r o o m
s u r f a c e s
N o .
o f
a g a r
M a x i -
p l a t e s m u m
No
f
on
S a m -
n o . o f
S u r f a c e
sam-
w h i c h
p l e a
c o l i f o r m s
pc o l i - p o s i t i v e
d e t e c t e d
p l e a
om
p o s i t i v e
o
f o r m s on
a
w e r e
s i n g l e
d e -
p l a t e
t e c t e d
W a l l s
5 4 1 1
2 0
5
F l o o r
1 2 0
3 1
2 6 > 1 0 0
S e a t ,
t o i l e t
7 0 2 7
3 8
1 5
R i m ,
t o i l e t 3 5
1 0
2 8
> 6 0
F l u s h h a n d l e
9 1 1 1
2
B a t h t u b s , s i n k s ,
1 2 5
6
5
>
1 0 0
c a b i n e t s ,
e t c .
a
R o d a c
p l a t e s
o f EMB
a g a r
w e r e
u s e d .
p u b l i c
b a t h r o o m s
were
s a m p l e d
f o r t h e
presence
o f c o l i f o r m s .
T h e r e s u l t s
are
s u m m a r i z e d i n
T a b l e
1 0 .
O v e r
2 0
b a t h r o o m s were t e s t e d
a n d
c o l i f o r m s were d e t e c t e d
i n
a l l ,
i n d i c a t i n g
t h a t
s u r f a c e c o n t a m i n a t i o n i n
t h e b a t h r o o m
i s
com-
mon.
DISCUSSION
C o n s i d e r a b l e
n u m b e r s
o f
b a c t e r i a
a n d
v i r u s e s
were s h o w n
t o
r e m a i n
i n t h e b o w l w a t e r
a f t e r
f l u s h i n g , a n d
e v e n c o n t i n u a l
f l u s h i n g c o u l d
n o t
r e m o v e
a
p e r s i s t e n t
f r a c t i o n . T h i s wa s a t t r i b -
u t e d t o
t h e a d s o r p t i o n o f t h e
o r g a n i s m s
t o
t h e
p o r c e l a i n s u r f a c e s o f t h e b o w l , w i t h
g r a d u a l
e l u t i o n o c c u r r i n g
a f t e r e a c h
f l u s h . T h i s a d -
s o r b e d f r a c t i o n
c o u l d
e x p l a i n t h e h e a v y
b a c t e -
r i a l
a e r o s o l s d e t e c t e d
b y
D a r l o w a n d
B a l e
( 6 )
a f t e r
t h e
s e c o n d
f l u s h
o f
t o i l e t s
s e e d e d w i t h
b a c t e r i a . I n
t o i l e t
b o w l
w a t e r s t e s t e d
b y
u s ,
c h l o r i n e
w a s u s u a l l y
a b s e n t
o r w a s
p r e s e n t
i n
v e r y
s m a l l
a m o u n t s ( < 1
m g / l i t e r ) ,
p r o b a b l y
d u e
t o i t s
r a p i d l o s s
t o t h e
a t m o s p h e r e .
I n
a d d i t i o n ,
o r g a n i c
m a t t e r
i n
t h e
s t o o l w o u l d c o m b i n e
w i t h
a n y f r e e c h l o r i n e
t h a t
m i g h t b e p r e s e n t .
T h u s , a
g r a d u a l b u i l d - u p o f b o t h b a c t e r i a a n d v i r u s e s
i n
t o i l e t s c o u l d
o c c u r
d u r i n g r e g u l a r u s e .
D r o p l e t s p r o d u c e d
b y f l u s h i n g
t o i l e t s
w e r e
f o u n d t o h a r b o r
b o t h b a c t e r i a a n d
v i r u s e s
p l a c e d i n
t h e
t o i l e t
b e f o r e f l u s h i n g .
T h e
a v e r a g e
human
s t o o l
w e i g h s
a p p r o x i m a t e l y
1 0 0
g a n d
c o n t a i n s a
t o t a l
o f
a b o u t
1 0 l 2
b a c t e r i a
( 1 8 ) ,
o f
w h i c h
1 0 i 0
o r m o r e
a r e
c o l i f o r m s ( 1 9 ) . I n i n -
f e c t e d
p e r s o n s , u p
t o
1 0 1
S a l m o n e l l a
( 1 9 )
a n d
1 0 8
t o 1 0 1 S h i g e l l a
( 1 4 )
h a v e
b e e n
d e t e c t e d
i n
t h e
s t o o l .
C o n c e n t r a t i o n s
a s
h i g h
a s 1 0 i 0
S a l m o -
n e l l a
p a r a t y p h i B
p e r
g o f
f e c e s h a v e b e e n
d e t e c t e d i n
c a r r i e r s
( 1 9 ) .
T h e n u m b e r o f
p o l i o -
v i r u s e s
p r e s e n t
i n
t h e s t o o l
o f i n f e c t e d
p e r s o n s
c a n
b e
a s
h i g h
a s
1 0 6 p e r
g o f
f e c e s , g i v i n g
a
t o t a l
o f 1 0 . i n t h e s t o o l
( 1 6 ) .
F o r t h e s e
v a l u e s ,
t h e
n u m b e r
o f i n f e c t i o u s
o r g a n i s m s e j e c t e d
f r o m
t h e
b o w l
w o u l d
r a n g e
f r o m
1 , 0 0 0
t o
o v e r
1 0 , 0 0 0
b a s e d
o n
d a t a
o b t a i n e d i n
t h i s
s t u d y .
O r g a n i s m s
c o l l e c t e d
o n
t h e
g a u z e
p r o b a b l y
r e p r e s e n t
t h o s e
c o n t a i n e d i n t h e
l a r g e r - s i z e d
d r o p l e t s
t h a t
q u i c k l y
s e t t l e o u t o n
s u r f a c e s
i n
t h e b a t h r o o m a n d d o n o t t a k e i n t o
a c c o u n t t h e
o r g a n i s m s p r e s e n t
i n
s m a l l e r
d r o p l e t s
w h i c h
ma y
b e a i r b o r n e f o r c o n s i d e r a b l e
l e n g t h s o f
t i m e .
T h e
d e t e c t i o n
o f c o l i f o r m
b a c t e r i a
a n d
v i r u s e s
f a l l i n g
o u t
o n t o
s u r f a c e s
i n
t h e
b a t h r o o m
a f t e r
f l u s h i n g
i n d i c a t e d t h a t
t h e s e
o r g a n i s m s
r e m a i n a i r b o r n e
l o n g e n o u g h
t o
s e t t l e o n s u r -
f a c e s
t h r o u g h o u t
t h e b a t h r o o m .
T h e
n u m b e r
o f
E . c o l i
d e t e c t e d o n t h e a g a r
p l a t e s i s p r o b a b l y
a
m i n i m a l
v a l u e s i n c e a i r b o r n e b a c t e r i a a r e
d a m -
a g e d
d u r i n g
a e r o s o l i z a t i o n
a n d
b y
e n v i r o n m e n -
t a l
s t r e s s e s , m a k i n g
g r o w t h
o n
s e l e c t i v e m e d i a
m o r e
d i f f i c u l t ( 1 3 ) .
T h e s e
d a t a a l s o d o
n o t
t a k e
i n t o
a c c o u n t
t h e
a c c u m u l a t i o n o f o r g a n i s m s
o n
t h e w a l l s
a n d
o t h e r
s u r f a c e s
o f
t h e b a t h r o o m .
T h e n u m b e r o f
v i r u s e s c a l c u l a t e d t o
b e
f a l l i n g
o u t
o n t o
t h e f l o o r
s u r f a c e
o f
t h e b a t h r o o m w a s
f o u n d t o b e o v e r a
l o g
g r e a t e r t h a n t h a t d e t e c t e d
w h e n
t h e
g a u z e
w a s
h e l d o v e r t h e
b o w l . T h i s
may
b e d u e t o
l a r g e n u m b e r s
o f v i r u s
b e i n g
p r e s e n t
i n
s m a l l e r - s i z e d
d r o p s
w h i c h d o
n o t
V O L .
3 0 ,
1 9 7 5
on S e p t em b er 1 0 ,2 0 1 3 b y g
u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
9/10
2 3 6 GERBA,
W A L L I S , A N D
MELNICK
i m p a c t
o n t o t h e g a u z e
d u r i n g
f l u s h i n g .
W h e r e a s
t h e n u m b e r
o f
b o t h
b a c t e r i a
a n d v i r u s e s
d e t e r -
m i n e d
t o b e
i m p a c t i n g
o n s u r f a c e s
w a s
l e s s
w h e n
t h e
b a t h r o o m
d o o r
a n d
v e n t s
w e r e l e f t
o p e n , i t
s h o u l d
b e p o i n t e d
o u t
t h a t
t h e o r g a -
n i s m s
n o t
s e t t l i n g
o u t
i n
t h e
r o o m
u n d e r t h e s e
c o n d i t i o n s
a r e
p r o b a b l y
b e i n g
c a r r i e d
t o
o t h e r
l o c a t i o n s
b y
a i r
c u r r e n t s .
T h e p r e s e n c e
o f
f e c a l
o r g a n i s m s
o n
b a t h r o o m
s u r f a c e s
i s
u n d o u b t e d l y
w i d e s p r e a d ,
a s e v i -
d e n c e d
b y t h e i s o l a t i o n
o f
c o l i f o r m b a c t e r i a
o n
s u r f a c e s
i n a l l
o f
t h e
b a t h r o o m s
s a m p l e d .
H u t c h i n s o n
( 1 2 ) d e t e c t e d
t h e p r e s e n c e
o f S h i -
g e l l a
s o n n e i
o n
b a t h r o o m
f l o o r s
a n d t o i l e t
s e a t s .
He
a l s o
f o u n d
t h a t t h i s
o r g a n i s m
c o u l d
p e r s i s t
f o r
a s
l o n g a s
1 7
d a y s
o n w o o d e n
w a t e r
c l o s e t
s e a t s .
Newsom
( 1 4 )
r e p o r t e d
t h a t
S a l m o n e l l a
s u r v i v e d f o r
1 1
d a y s
a f t e r
d e s i c c a t i o n
w h e n
s u s p e n d e d
i n
e i t h e r t a p w a t e r
o r
f e c e s .
I n
t h i s
p r e s e n t
s t u d y ,
l a r g e
n u m b e r s
o f c o l i f o r m
b a c t e -
r i a
w e r e
f o u n d o n
s e v e r a l
o c c a s i o n s
u n d e r
s h a m -
p o o b o t t l e s
i n b a t h r o o m s ,
w h i c h
m i g h t i n d i c a t e
t h a t r e g r o w t h
o r
p r o l o n g e d
p e r s i s t e n c e
o f
t h e s e
o r g a n i s m s
ma y
o c c u r
w h e r e
o r g a n i c
m a t e r i a l
h a s
a c h a n c e
t o
a c c u m u l a t e .
I n
a d d i t i o n ,
e n -
t e r o v i r u s e s , a s
w e l l a s
m e m b e r s
o f t h e
a d e n o v i -
r u s
a n d
r e o v i r u s
g r o u p s ,
h a v e
b e e n f o u n d
t o
s u r v i v e
d e s i c c a t i o n
o n s u r f a c e s
( 4 ) .
D o s e s o f
l e s s t h a n
1 0 2
S h i g e l l a f l e x n e r i
h a v e
b e e n f o u n d
t o
b e
c a p a b l e
o f
i n i t i a t i n g i n f e c t i o n
i n
ma n ( 9 ) .
A l s o ,
D a r l o w
e t a l . ( 7 )
h a v e
s h o w n
t h a t
t h e
l e t h a l
d o s e o f
S a l m o n e l l a
t y p h i m u r i u m
i n m i c e
w a s
l o w e r w h e n
t h e y
w e r e i n f e c t e d
b y
i n h a l a t i o n r a t h e r
t h a n
i n g e s t i o n .
W i t h
v i r u s ,
h o w e v e r ,
t h e
m i n i m a l
i n f e c t i o u s
d o s e
f o r
h u -
m a n s may
b e a s
l o w
a s
o n e t i s s u e c u l t u r e
i n f e c t i o u s
d o s e
( 1 5 ) .
T h u s ,
i t w o u l d a p p e a r
t h a t
t h e n u m b e r s
o f b a c t e r i a
a n d v i r u s e s
e j e c t e d
f r o m
t h e t o i l e t
a r e
s u f f i c i e n t l y
l a r g e
t o i n i t i a t e
i n f e c t i o n ,
e s p e c i a l l y
i n
t h e
c a s e
o f v i r u s e s .
I n
a
s t u d y
o f
a i r b o r n e
t r a n s m i s s i o n
o f
c o x s a c k -
i e v i r u s t y p e 2 1 ,
C o u c h
e t
a l .
( 5 )
d e t e c t e d
o n l y
1
5 0
t i s s u e
c u l t u r e
i n f e c t i o u s
d o s e
p e r
3 . 5
f t 3
( 0 . 1 0
m i )
i n
a b a r r a c k s
i n w h i c h
a e r o s o l
t r a n s -
m i s s i o n
o f
t h e
v i r u s
b e t w e e n
h u m a n s
o c c u r r e d .
I n a n a r m y
b a r r a c k s
i n
w h i c h
t r a n s m i s s i o n
o f
a d e n o v i r u s
w a s
o c c u r r i n g ,
a i r
s a m p l i n g
r e v e a l e d
t h e
p r e s e n c e
o f
o n l y
1
5 0
t i s s u e
c u l t u r e
i n f e c t i o u s d o s e
i n 9 2 0
f t 3
( 2 5 . 7 6 m i n )
o f
a i r
( 2 ) .
T h e r e s u l t s
o f
o u r
s t u d y
w o u l d
s e e m
t o i n d i c a t e
t h a t
g r e a t e r
c o n c e n t r a t i o n s
o f
v i r u s
w o u l d
e x i s t
a s
a e r o s o l s
i n
b a t h r o o m s
i n w h i c h
i n f e c t i o u s
m a t e r i a l
h a s
b e e n f l u s h e d .
T h e s p r e a d
o f
v i r a l
d i s e a s e
b y
a e r o s o l s
f r o m
t o i l e t s may
t a k e
o n
a d d e d
i m p o r t a n c e
i n t h o s e
v i r a l
d i s e a s e s
i n
w h i c h
l o w n u m b e r s
o f v i r u s e s
a r e
e x c r e t e d
i n
n a s o p h a r y n g e a l
s e c r e t i o n s
a s c o m p a r e d
t o
t h e
a m o u n t
e x c r e t e d
i n t h e f e c e s .
I n
a d d i t i o n ,
t h e
A P P L . M I C R O B I O L .
o v e r a l l
i m p o r t a n c e
o f e n t e r i c
v i r u s
t r a n s m i s s i o n
b y r e s p i r a t o r y
s e c r e t i o n s
i s s t i l l
i n
d i s p u t e .
F o r
e x a m p l e ,
t h e
s p r e a d
o f
p o l i o v i r u s
w i t h i n
f a m i
l i e s
w h e n
p h a r y n g e a l
e x c r e t i o n
o c c u r r e d
d i f -
f e r e d
l i t t l e
f r o m
t h a t f o l l o w i n g
p u r e l y
f e c a l
e x c r e t i o n
( 1 0 ) .
A l s o ,
r e c e n t
s t u d i e s
w i t h
a d e n o -
v i r u s t y p e
4 i n d i c a t e
t h a t f e c a l
s o u r c e s
ma y
b e
m o r e
i m p o r t a n t
t h a n
r e s p i r a t o r y
s o u r c e s
i n
t h e
s p r e a d
o f t h i s
v i r u s
( 1 0 ) .
T h e
s i g n i f i c a n c e
o f
e n t e r i c
v i r u s
d i s e a s e
t r a n s m i s s i o n
b y
c o n t a c t
w i t h
s u r f a c e s h a r b o r i n g
i n f e c t i o u s
m a t e r i a l
s h o u l d
n o t
b e o v e r l o o k e d ,
a s
e v i d e n c e d
b y
t h e
r e c e n t
f i n d i n g s
o f
H e n d l e y
e t
a l . ( 1 1 )
o n t h e
t r a n s m i s s i o n
o f
r h i n o v i r u s
f r o m
f o m i t e s
t o t h e
h a n d s
a n d s e l f - i n o c u l a t i o n
o f
t h e
e y e s
a n d n o s e .
A d d i t i o n a l
e v i d e n c e
w o u l d
b e
n e c e s s a r y
t o
s u b s t a n t i a t e
t h e
r o l e
o f
a e r o s o l s
i n
t h e e p i d e m i o l o g y
o f d i s e a s e
t r a n s m i s s i o n b y
t o i l e t s ,
b u t t h e
r e s u l t s
o f t h i s s t u d y
i n d i c a t e
t h a t
i t
a p p e a r s
t o
b e
a d i s t i n c t
p o s s i b i l i t y .
LITERATURE
CITED
1 .
A d a m s ,
M .
H .
1 9 5 9 .
B a c t e r i o p h a g e s .
I n t e r s c i e n c e
P u b -
l i s h e ' s ,
New Y o r k .
2 . A r t e n s t e i n ,
M.
S . ,
a n d
W . S .
M i l l e r . 1 9 6 6 .
A i r
s a m p l i n g
f o r r e s p i r a t o r y
d i s e a s e
a g e n t s
i n
a r m y
r e c r u i t s .
B a c t e -
r i o l .
R e v . 3 0 : 5 7 1 - 5 7 2 .
3 .
B o u n d ,
W.
H . ,
a n d
R . I .
A t k i n s o n .
1 9 6 6 . B a c t e r i a l
a e r o s o l
f r o m
w a t e r
c l o s e t s .
A
c o m p a r i s o n
o f t w o t y p e s
o f
p a n
a n d
t w o
t y p e s
o f c o v e r .
L a n c e t
i : 1 3 6 9 - 1 3 7 0 .
4 . B u c k l a n d ,
F .
E . ,
a n d
D .
A .
J .
T y r r e l l .
1 9 6 2 .
L o s s
o f
i n f e c t i v i t y
o n
d r y i n g
v a r i o u s
v i r u s e s . N a t u r e ( L o n d o n )
1 9 5 : 1 0 6 3 - 1 0 6 4 .
5 .
C o u c h ,
R .
B . ,
R . G .
D o u g l a s ,
J r . ,
K .
M .
L i n d g r e n ,
P .
J .
G e r o n e ,
a n d
V .
K n i g h t .
1 9 7 0 .
A i r b o r n e
t r a n s m i s s i o n
o f
r e s p i r a t o r y
i n f e c t i o n
w i t h c o x s a c k i e v i r u s
A
t y p e
2 1 .
Am.
J .
E p i d e m i o l . 9 1 : 7 8 - 8 6 .
6 .
D a r l o w ,
H .
M . ,
a n d
W. R . B a l e .
1 9 5 9 .
I n f e c t i v e
h a z a r d s
o f
w a t e r - c l o s e t s .
L a n c e t
i : 1 1 9 6 - 1 2 0 0 .
7 . D a r l o w ,
H . M . ,
W.
R . B a l e ,
a n d
G .
B .
C a r t e r .
1 9 6 1 .
I n f e c t i o n
o f m i c e b y
t h e r e s p i r a t o r y
r o u t e
w i t h
S a l m o -
n e l l a t y p h i m u r i u m .
J .
H y g .
5 9 : 3 0 3 - 3 0 8 .
8 . D a v i s ,
J .
E . ,
a n d
R .
L .
S i n s h e i m e r .
1 9 6 3 . T h e
r e p l i c a t i o n
o f
b a c t e r i o p h a g e
M S - 2 .
I . T r a n s f e r
o f
p a r e n t a l
n u c l e i c
a c i d
t o
p r o g e n y
p h a g e .
J . M o l . B i o l . 6 : 2 0 3 - 2 0 7 .
9 .
D u P o n t ,
H .
L . ,
R . B . H o r n i c k ,
M .
J . S n y d e r ,
J .
P .
L i b o n a t i ,
S .
B . F o r m a l ,
a n d
E . J . G a n g a r o s a .
1 9 7 2 .
I m m u n i t y
i n
s h i g e l l o s i s .
I I . P r o t e c t i o n
i n d u c e d
b y
o r a l
l i v e v a c c i n e
o r
p r i m a r y
i n f e c t i o n .
J .
I n f e c t .
D i s .
1 2 5 : 1 2 - 1 6 .
1 0 .
F o x ,
J .
P . 1 9 7 3 .
I n t r o d u c t i o n a n d s p r e a d
o f
r e s p i r a t o r y
v i r a l
p a t h o g e n s
i n
f a m i l i e s ,
p .
4 8 7 - 4 9 3 .
I n
J .
F .
H e r s
a n d
K .
C .
W i n k l e r
( e d . ) ,
A i r b o r n e
t r a n s m i s s i o n
a n d
a i r b o r n e
i n f e c t i o n . J .
W i l e y
a n d
S o n s ,
New
Y o r k .
1 1 . H e n d l e y ,
J .
O . ,
R .
P .
W e n z e l ,
a n d J .
M.
G w a l t n e y ,
J r .
1 9 7 3 . T r a n s m i s s i o n
o f
r h i n o v i r u s
c o l d s
b y
s e l f - i n o c u l a -
t i o n .
New E n g l .
J . M e d . 2 8 8 : 1 3 6 1 - 1 3 6 4 .
1 2 . H u t c h i n s o n ,
R . I . 1 9 5 6 . S o m e
o b s e r v a t i o n s
o n t h e
m e t h o d
o f
t h e
s p r e a d
o f s o n n e
d y s e n t e r y .
M o n .
B u l l .
M i n i s t .
H e a l t h
P u b l i c
H e a l t h
L a b .
S e r v .
1 5 : 1 1 0 - 1 1 8 .
1 3 .
K i n g s o n ,
D . 1 9 7 1 .
S e l e c t i v e
m e d i a
i n a i r
s a m p l i n g :
a
r e v i e w .
J .
A p p l .
B a c t e r i o l .
3 4 : 2 2 1 - 2 3 2 .
1 4 . N e w s o m ,
S .
W.
B .
1 9 7 2 .
M i c r o b i o l o g y
o f
h o s p i t a l
t o i l e t s .
L a n c e t i i : 7 0 0 - 7 0 3 .
1 5 . P l o t k i n ,
S .
A . ,
a n d
M .
K a t z . 1 9 6 7 .
M i n i m a l
i n f e c t i v e
d o s e s
o f
v i r u s e s
f o r
ma n
b y
t h e
o r a l
r o u t e , p .
1 5 1 - 1 5 6 .
I n
G .
B e r g ( e d . ) ,
T r a n s m i s s i o n
o f
v i r u s e s
b y
t h e
w a t e r
on S e p t em b er 1 0 ,2 0 1 3 b y g
u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/
8/9/2019 Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms
10/10
MICROBIOLOGICAL
HAZARDS
OF
HOUSEHOLD
TOILETS
2 3 7
r o u t e .
J .
W i l e y
a n d
S o n s ,
New
Y o r k .
1 6 .
S a b i n , A . B .
1 9 5 5 .
B e h a v i o r
o f
c h i m p a n z e e - a v i r u l e n t
p o l i o m y e l i t i s
v i r u s e s
i n
e x p e r i m e n t a l l y
i n f e c t e d
human
v o l u n t e e r s .
Am .
J .
M e d . S c i .
2 3 0 : 1 - 8 .
1 7 .
S o b s e y , M.
D . , C .
W a l l i s ,
M .
H e n d e r s o n ,
a n d J .
L .
M e l n i c k .
1 9 7 3 . C o n c e n t r a t i o n
o f
e n t e r o v i r u s e s f r o m
l a r g e
v o l u m e s
o f w a t e r . A p p l . M i c r o b i o l .
2 6 : 5 2 9 - 5 3 4 .
1 8 .
S t a n i e r , R .
Y . ,
M.
D o u d o r o f f ,
a n d
E . A .
A d e l b e r g .
1 9 7 0 .
T h e
m i c r o b i a l w o r l d .
P r e n t i c e - H a l l ,
E n g l e w o o d
C l i f f s ,
N . J .
1 9 .
T h o m s o n , S .
1 9 5 4 . T h e
n u m b e r
o f
b a c i l l i
h a r b o u r e d
b y
e n t e r i c
c a r r i e r s .
J .
H y g . 5 2 : 6 7 - 7 0 .
2 0 .
W a l l i s , C . ,
S .
G r i n s t e i n ,
J .
L
M e l n i c k ,
a n d J .
E .
F i e l d s .
1 9 6 9 .
C o n c e n t r a t i o n
o f
v i r u s e s
f r o m
sewage a n d
e x c r e t a
on
i n s o l u b l e
p o l y e l e c t r o l y t e s .
A p p l .
M i c r o b i o l .
1 8 : 1 0 0 7 - 1 0 1 4 .
2 1 .
W a l l i s ,
C . ,
M .
H e n d e r s o n ,
a n d
J .
L .
M e l n i c k .
1 9 7 2 .
E n t e r o v i r u s
c o n c e n t r a t i o n
on
c e l l u l o s e
m e m b r a n e s .
A p p l .
M i c r o b i o l .
2 3 : 4 7 6 - 4 8 0 .
2 2 .
W a l l i s ,
C . ,
a n d
J .
L .
M e l n i c k .
1 9 6 7 .
C o n c e n t r a t i o n
o f
e n t e r o v i r u s e s
on
m e m b r a n e
f i l t e r s .
J . V i r o l .
1 : 4 7 2 - 4 7 7 .
V O L .
3 0 , 1 9 7 5
on S e p t em b er 1 0 ,2 0 1 3 b y g
u e s t
h t t p: / / a em. a s m. or g /
D ownl o a d e d f r om
http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/http://aem.asm.org/