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would be reasonable to assume that cysts, similar to spores, tics and disinfectants has been reported. Of the mechanisms
take up fewer disinfectant molecules from solution than do that have been studied, the most significant are clearly intrin-
vegetative forms. sic, in particular the ability to sporulate, adaptation of pseudo-
Some recent studies have compared the responses of cysts monads, and the protective effects of biofilms. In these cases,
and trophozoites of Acanthamoeba castellanii to disinfectants resistance may be incorrectly used and tolerance, defined
used in contact lens solutions and monitored the development as developmental or protective effects that permit microorgan-
of resistance during encystation and the loss of resistance dur- isms to survive in the presence of an active agent, may be more
ing excystation (251 255). The lethal effects of chlorhexidine correct. Many of these reports of resistance have often pa-
and of a polymeric biguanide were time and concentration de- ralleled issues including inadequate cleaning, incorrect prod-
pendent, and mature cysts were more resistant than preencyst- uct use, or ineffective infection control practices, which cannot
ment trophozoites or preexcystment cysts. The cyst wall ap- be underestimated. Some acquired mechanisms (in particular
peared to act as a barrier to the uptake of these agents, thereby with heavy-metal resistance) have also been shown to be clin-
presenting a classical type of intrinsic resistance mechanism ically significant, but in most cases the results have been spec-
170 MCDONNELL AND RUSSELL CLIN. MICROBIOL. REV.
TABLE 16. Viral classification and response to some disinfectantsa a mutant of Pseudomonas aeruginosa. Appl. Microbiol. 21:1058 1063.
3. Adler-Storthz, K., L. M. Sehulster, G. R. Dreesman, F. B. Hollinger, and
Effects of J. L. Melnick. 1983. Effect of alkaline glutaraldehyde on hepatitis B virus
disinfectantsc
antigens. Eur. J. Clin. Microbiol. 2:316 320.
Viral Lipid
4. Agerton, T., S. Valway, B. Gore, C. Pozsik, B. Plikaytis, C. Woodley, and I.
group envelopeb Examples of viruses
Lipo- Broad-
Onorato. 1997. Transmission of a highly drug-resistant strain (strain W1) of
philic spectrum
Mycobacterium tuberculosis. JAMA 278:1073 1077.
5. Ahonkhai, I., and A. D. Russell. 1979. Response RP1 and RP1 strains of
A HSV, HIV, Newcastle disease virus, S S
Escherichia coli to antibacterial agents and transfer of resistance to Pseudo-
rabies virus, influenza virus
monas aeruginosa. Curr. Microbiol. 3:89 94.
6. Alexandre, H., I. Rousseaux, and C. Charpentier. 1994. Relationship be-
B Non-lipid picornaviruses (poliovirus, R S
tween ethanol tolerance, lipid composition and plasma membrane fluidity
Coxsackie virus, echovirus)
in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol. Lett.
124:17 22.
C Other larger nonlipid viruses R S
7. Alfa, M. J., and D. L. Sitter. 1994. In-hospital evaluation of orthophthal-
(adenovirus, reovirus) aldehyde as a high level disinfectant for flexible endoscopes. J. Hosp. Infect.
26:15 26.
a
Data from reference 259; see also reference 444. For information on the
8. Al-Masaudi, S. B., M. J. Day, and A. D. Russell. 1991. Antimicrobial
inactivation of poliovirus, see reference 514.
resistance and gene transfer in Staphylococcus aureus. J. Appl. Bacteriol. 70:
b
Present ( ) or absent ( ).
279 290.
c
Lipophilic disinfectants include QACs and chlorhexidine. S, sensitive; R,
9. Alqurashi, A. M., M. J. Day, and A. D. Russell. 1996. Susceptibility of some
resistant.
strains of enterococci and streptococci to antibiotics and biocides. J. Anti-
microb. Chemother. 38:745.
10. Anderson, R. L. 1989. Iodophor antiseptics: intrinsic microbial contamina-
tion with resistant bacteria. Infect. Control Hosp. Epidemiol. 10:443 446.
ulative. Increased MICs have been confirmed, in particular for
11. Anderson, R. L., J. H. Carr, W. W. Bond, and M. S. Favero. 1997. Suscep-
staphylococci. However, few reports have further investigated
tibility of vancomycin-resistant enterococci to environmental disinfectants.
increased bactericidal concentrations or actual use dilutions of Infect. Control Hosp. Epidemiol. 18:195 199.
12. Anderson, R. L., B. W. Holland, J. K. Carr, W. W. Bond, and M. S. Favero.
products, which in many cases contain significantly higher con-
1990. Effect of disinfectants on pseudomonads colonized on the interior
centrations of biocides, or formulation attributes, which can
surface of PVC pipes. Am. J. Public Health 80:17 21.
increase product efficacy; in a number of cases, changes in the
13. Anderson, R. L., R. W. Vess, J. H. Carr, W. W. Bond, A. L. Panlilio, and
MICs have actually been shown not to be significant (9, 88, 89,
M. S. Favero. 1991. Investigations of intrinsic Pseudomonas cepacia con-
tamination in commercially manufactured povidone-iodine. Infect. Control
319, 428). Efflux mechanisms are known to be important in
Hosp. Epidemiol. 12:297 302.
antibiotic resistance, but it is questionable if the observed in-
14. Anderson, R. L., R. W. Vess, A. L. Panlilio, and M. S. Favero. 1990.
creased MICs of biocides could have clinical implications for
Prolonged survival of Pseudomonas cepacia in commercially manufactured
hard-surface or topical disinfection (423, 428). It has been
povidone-iodine. Appl. Environ. Microbiol. 56:3598 3600.
15. Apostolov, K. 1980. The effects of iodine on the biological activities of
speculated that low-level resistance may aid in the survival of
myxoviruses. J. Hyg. 84:381 388.
microorganisms at residual levels of antiseptics and disinfec-
16. Ascenzi, J. M. 1996. Glutaraldehyde-based disinfectants, p. 111 132. In
tants; any possible clinical significance of this remains to be
J. M. Ascenzi (ed.), Handbook of disinfectants and antiseptics. Marcel
tested. With growing concerns about the development of bio-
Dekker, Inc., New York, N.Y.
cide resistance and cross-resistance with antibiotics, it is clear 17. Ayliffe, G. A. J., D. Coates, and P. N. Hoffman. 1993. Chemical disinfection
in hospitals, 2nd ed. Public Health Laboratory, London, England.
that clinical isolates should be under continual surveillance and
18. Ayres, H., J. R. Furr, and A. D. Russell. 1993. A rapid method of evaluating
possible mechanisms should be investigated.
permeabilizing activity against Pseudomonas aeruginosa. Lett. Appl. Micro-
It is also clear that antiseptic and disinfectant products can
biol. 17:149 151.
vary significantly, despite containing similar levels of biocides,
19. Azachi, M., Y. Henis, R. Shapira, and A. Oren. 1996. The role of the outer
membrane in formaldehyde tolerance in Escherichia coli VU3695 and
which underlines the need for close inspection of efficacy
Halomonas sp. MAC. Microbiology 142:1249 1254.
claims and adequate test methodology (183, 423, 428). In ad-
20. Baillie, L. W. J., J. J. Wade, and M. W. Casewell. 1992. Chlorhexidine
dition, a particular antiseptic or disinfectant product may be
sensitivity of Enterococcus faecium resistant to vancomycin, high levels of
better selected (as part of infection control practices) based on
gentamicin, or both. J. Hosp. Infect. 20:127 128.
particular circumstances or nosocomial outbreaks; for exam- 21. Bailly, J.-L., M. Chambron, H. Peigue-Lafeuille, H. Laveran, C. de
Champs, and D. Beytout. 1991. Activity of glutaraldehyde at low concen-
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