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Neisseria Gonorrhoeae II JOURNAL OF BACrERIOLOGY, Sept. 1968, p. 596-605 Vol. 96, No. 3 Copyright © 1968 American Society for Microbiology Printed in U.S.A. Neisseria gonorrhoeae II. Colonial Variation and Pathogenicity During 35 Months In Vitro DOUGLAS S. KELLOGG, JR., IRUN R. COHEN, LESLIE C. NORINS, ARNOLD L. SCHROETER, AND GILBERT REISING Venereal Disease Research Laboratory, National Communicable Disease Center, Atlanta, Georgia 30333 Received for publication 15 June 1968 During 35 months of selective in vitro cultivation, Neisseria gonorrhoeae cells re- tained their virulence for humans and were shown to be closely related to a particu- lar colonial morphology. Saline-autoagglutinability was the only other characteristic distinguishing virulent from avirulent cells. Human responses to challenge with cells of the different colonial types were studied for their relationships to virulence or avirulence. Since its initial cultivation in 1882, Neisseria (after 69 selective transfers in vitro), cells of colo- gonorrhoeae has been extensively studied as an nial type Tl were found to be virulent and cells of academic challenge and as a practical medical colonial type T4 were found to be avirulent for diagnostic problem. In spite of such study, little human volunteers. Virulence testing could not be had been ascertained about the immunological attempted with cells of either colonial type T2 response of humans to a gonococcal infection. or T3 after 69 selective transfers in vitro because Immunity appeared to be transient or limited in of time and space limitations. At 38 transfers, in- nature as evidenced by repeated reinfections and fections resulted from inoculations of cells of the development of chronic conditions and car- colonial types Ti, T2, T3, and T4; however, the rier states. Antibody production could be detected appearance of signs and symptoms was paralleled by complement-fixation procedures using ex- by an alteration in recovered colony types from tracted antigens; however, there was not a close T2, T3, or T4 to T1. At that point, Ti colonies correlation of serological reactivity with infection could still be isolated from cultures of colonial (13, 19). Studies of the antigenic mosaic of N. types T2, T3, and T4. This paper presents the gonorrhoeae demonstrated antigenic variation results of further studies of virulence of N. gonor- among strains and considerable sharing of anti- rhoeae for humans, and certain characteristics of gens with other species of Neisseria as well as the infectious process and the organisms them- other genera of bacteria (24). Most studies of N. selves which may be related to their virulence and gonorrhoeae antigens were done with strains which overall interaction with the host. had been carried in vitro long enough to obtain a sufficient number of cells for antigenic analysis. MATERIALS AND METHODS In vitro cultivation of N. gonorrhoeae resulted in a N. gonorrhoeae strain F62 was originally isolated by conversion of normal saline autoagglutinability this laboratory in 1962 (12). Primary isolates were ob- from rough to smooth, possibly due to an anti- tained at the Fulton County Health Department, genic alteration, and a loss of virulence. Since Atlanta, Ga., through the assistance and cooperation man was the only known host for N. gonorrhoeae, of John H. Tiedemann. All colonial lines of strains and usually was infected only by venereal contact, were passaged by loop transfer of individual colonies little was known about virulence of N. gonor- selected by morphological characteristics observed by rhoeae for of a means of an AO Cycloptic dissecting microscope with except the possible involvement diffused, angled light transmitted from below up potent endotoxin which avirulent strains were through the medium. Measurements of colonial di- known to possess. Progress in ascertaining basic ameter during iron studies were accomplished with facts about N. gonorrhoeae was hampered by a 20-fold magnification and an oculhr micrometer. On double deficiency: lack of an experimental animal three separate occasions, approximately 100 well- and lack of a marker associated with virulence. In isolated colonies were measured at each compound 1963, four clonal types were described for N. level under study. All transfers were made after 16 to 20 hr of incubation at 35 C under increased carbon gonorrhoeae and a correlation was demonstrated dioxide tension (candle extinction). G C Medium Base between colonial morphology and virulence with (GCB; Difco), enriched with a defined supplement two of the four colonial types (12). At that time (DSF), was used for the isolation and cultivation of 596 VOL. 96, 1968 VIRULENT N. GONORRHOEAE IN VITRO 597 all strains (22). The defined supplement was added to loop sample of the urethral canal surfaces were ob- the basal medium at 43 to 45 C just before pouring. tained. Each subject received a full 2-mm bacteriologi- When hemolyzed whole rabbit blood (5%) supple- cal loop of the desired colonial type of cells picked ment was used, it was added with the defined supple- only from areas free of contaminating colonial types. ment. In examinations of pharyngeal and rectal speci- Each inoculum was inserted approximately 2 to 3 mens, a selective medium was used (20). The fermen- inches (5 to 7.6 cm) into the urethra, and the subject tation medium utilized for confirmation of species was instructed not to urinate for several hours. Daily identity was described by White and Kellogg (23). The samples for examinations were taken by inserting the synthetic medium used was described by Gould, Kane, loop into the urethra. Each daily specimen from each and Mueller (8). Demonstration of capsules was at- subject was examined by FA techniques and cultural tempted by a technique in which suspensions of N. procedures (colony morphology, oxidase reactivity, gonorrhoeae in 10% sterile skim milk are examined sugar fermentations, and Gram reaction) to identify with fixed-phase optics (6). The fluorescent-antibody the infecting organism as N. gonorrhoeae. After ter- (FA) procedures applied to direct smears, and/or mination of the infection study, each subject was ade- smears of cultures, were described by White and Kel- quately treated with either aqueous procaine penicillin logg (22). The precipitin procedure for serum anti- G or oxytetracycline. The subject was examined 24, bodies and control sera production was that described 48, and 72 hr after treatment for signs of infection, and by Reising and Kellogg (16). The oxidase procedure the urethra, urine, and prostate were sampled for the was performed as described in U.S. Public Health presence of N. gonorrhoeae by FA and cultural pro- Service Publication 499 (21). Assays for the presence cedures. Volunteers were not released from the study of hemolysin, coagulase, and fibrinolysin were con- ward until three successive daily examinations were ducted according to standard procedures described negative for N. gonorrhoeae by all procedures. Blood for other microorganisms (9). Toxic potential of the specimens for serological examination were collected cell types was assayed by intraperitoneal injection of at intervals over the next 3 months. equivalent numbers of each cell type into CFW mice. Antibiotic susceptibilities ofthe strains used for volun- RESULTS teer inoculation were determined by James D. Thayer of the Venereal Disease Research Laboratory. Colonial morphology in N. gonorrhoeae. The After 17 months ofpassage, the four colony types of four colonial types originally described have been N. gonorrhoeae (TI, T2, T3, and T4) were tested for found to represent the most stable morphological virulence with separate groups of four subjects. After configurations for the conditions of their cultiva- 35 months of passage, only the colony; type Ti was tion. There are a variety of temporary morpho- tested for virulence and a group of 10 subjects was logical variations which appear as a result of used. environmental alterations, as well as some varia- All subjects were male volunteers at Atlanta, Ga. tions which are capable of perpetuating them- Before examination as a possible subject for the study, selves under the conditions of selective transfer. each volunteer provided assurance that he understood the purpose of the experimentation and the possible As a consequence, in the selective transfer of the risks involved. Selection of the subjects for the study colonial types, we have adhered as closely as pos- required satisfaction of the following criteria. He must sible to the originally described characteristics in have been between ages 21 and 45 years and available picking colonies for transfer. The original strain for a poststudy observation period of 6 months. He (F62) colonial types, which have been carried as must have been acceptable from the standpoint of separate entities for 3.5 years, are morphologically mentality, psyche, and ability to cooperate. To be ac- very similar to colonial types obtained from sam- ceptable, the subject must not have had a gonococcal ples that were frozen or lyophilized in 1963. The infection within the previous 3 months nor have been two colonial Ti and obtained from an asymptomatic carrier of N. gonorrhoeae; neither types, T2, could he harbor an acute or chronic disease or psy- patients are characterized by their glistening con- chogenic disorder. Freedom from gonococcal infection vexity, dark-brown to black coloration, and small or carrier state was determined by clinical and labora- size (0.5 mm and 0.4 mm, respectively; Fig. 1). tory
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