Risk Factors for Carriage of Neisseria meningitidis during an Outbreak in Wales

Patricia E. Fitzpatrick,* Roland L. Salmon,* Paul R. Hunter,† Richard J Roberts,‡ and Stephen R. Palmer*
*PHLS Communicable Disease Surveillance Centre (Wales), Cardiff, United Kingdom; †Chester Public Health Laboratory, Chester, United Kingdom; and ‡North Wales Health Authority, Mold, United Kingdom

Outbreaks of meningococcal disease, although rare, may have become more common in the United Kingdom, particularly among teenagers and young adults (1-3). In an investigation of a school-based outbreak in north Wales, extensive nasopharyngeal swabbing and subtyping allowed comparison of risk factors for carriage of the epidemic strain of Neisseria meningitidis B15 P1.16 and carriage of other meningococci.

On consecutive days in May 1996, two cases of meningococcal disease were reported in a single year group (year 11, ages 15 to 16 years) in a large (760 students) secondary school. One case was confirmed as due to N. meningitidis group B, type 15 P1.16. The second involved characteristic clinical symptoms, although blood culture and polymerase chain reaction (PCR) of serum were negative. In addition, five cases of meningococcal disease from the surrounding areas (total population 8,000) had been reported in the preceding 11 months. Three of these cases were in students of the school. One had been confirmed as N. meningitidis B15 P1.16 and one as serogroup C. The observed incidence of notified disease in England and Wales for 1995 was 3.7 per 100,000 and of culture-confirmed disease 2.9 per 100,000 total population (4). We conducted an investigation to determine the prevalence of N. meningitidis B15 P1.16 carriage in the school and examine the associated risk factors.

The Study

Throat swabs from students and staff were spread onto 5% Columbia blood agar containing polymyxin 25,000 units/L and vancomycin 3 mg/L. Primary incubation was conducted at 37°C for 48 hours in 10% CO₂. Plates showing preliminary growth were sent to the Meningococcal Reference Unit at Manchester Public Health Laboratory for further examination and serotyping. Rifampicin was given to students in year 11, which included all those subsequently found to be carriers of the epidemic strain.

Epidemiology

All students from whom a throat swab was taken were asked to complete a questionnaire about personal and household details, lifestyle and social behavior (including travel), and health. A household density ratio was calculated from the ratio of number of household members to the number of rooms in the house. Socioeconomic background was determined by occupation of the head of the household, according to the Office of Population Census and Surveys classification of occupations (5). As stress has been proposed as a risk factor for meningococcal disease (6), we asked about stressful events in the month before the diagnosis of the index cases (e.g., a death in the family, household move, or bad news).

Univariate analysis of risk factors for meningococcal carriage was performed by using Epi-Info (7); the chi-square test was used for statistical significance. Multivariate analysis of carriage of N. meningitidis was performed with SAS (SAS Institute Inc., Cary, NC); variables from univariate analysis were entered into a forward stepwise logistic regression, and conditional odds ratios and 95% confidence intervals were calculated for the resulting significant variables.

Swabs were taken from 744 (97.8%) of 760 pupils at the school. No pupil had received prior antimicrobial chemoprophylaxis. N. meningitidis was cultured from throat swabs of 60 (7.9%) students; 33 (55%) were in year 11. Of 17 group B isolates, 12 were type B15P1.16 (Table 1). Of 626 students (83.4%) who completed questionnaires, N. meningitidis was isolated from 53 students (8.5%) (Table 1).

Table 1. Subtyping of Neisseria meningitidis isolates in a Welsh secondary school

		Student group
		Questionnaire	Rate of
Subtype	Overall	completed	carriage (%)
B	17a	14	2.2
29E	7	6	0.9
C	4	4	0.5
Y	4	4	0.5
Z	2	0	0.3
W135	1	1	0.1
Nontypable	26	24	3.5
Total	61a	53	8.1
aIncluding isolate from the single N. meningitidis-positive teacher.

The rate of meningococcal carriage was significantly higher in students >14 years of age (Table 2). The proportion of carriers also increased with year in school (chi-square for linear trend 44.3; p < 0.001). Although having a stressful event within the previous 3 months was not associated with carriage, specifically receiving bad news was.

 

Table 2. Personal, family, and household factors and meningococcal carriage
						Exposed		Nonexposed
	Exposeda		Nonexposed
							B15		B15
	Meningo-		Meningo-		Odds	B15	P1.16	B15	P1.16	Odds
	coccal	Non-	coccal	Non-	ratio	P1.16	non-	P1.16	non-	ratio
Variable	carrier	carrier	carrier	carrier	(95% CI)	carrier	carrier	carrier	carrier	(95% CI)
Age >14	40	201	13	372	5.69b	11	230	0	384	Undefb
					(2.87-11.49)
Male sexc	31	267	22	304	1.60	9	289	2	324	5.04b
					(0.88-2.95)					(1.01-34.07)
Low socioeconomic	21	256	32	317	0.81	3	274	8	341	0.47
conditions					(0.67-2.29)					(0.10-1.95)
Shared bedroomc	13	106	40	466	1.43	4	115	7	499	2.48
					(0.69-2.90)					(0.60-9.62)
Household ratio >0.5	39	382	14	191	1.39	7	414	4	201	0.85
					(0.71-2.76)					(0.22-3.53)
>One child <5 yrs old	1	41	52	532	0.25	11	573	0	42	Undef
in same household
					(0.01-1.74)
Pet animalc	33	408	20	161	0.65	6	435	5	176	0.49
					(0.35-1.22)					(0.13-1.88)
aExposure to index patient.          bp< 0.05.          cData missing.

 
Students who reported that they had smoked cigarettes or lived with a smoker were more likely to carry meningococci (Table 3). Students in the same two classerooms and the same year as the index patients were more likely to carry N. meningitidis. Attendance at an informal party held by year 11 students 10 days before onset of illness was associated with carriage (Table 3). This informal gathering had no list of invitees; therefore, the number of those who attended but did not have throat swabs taken is not known.

Being in a sports team or regular attendance at youth clubs, Sunday schools, cubs, scouts, brownies, or guides was not associated with carriage, nor was recent travel.

Students who had been in regular contact with one of the patients were more likely to be carriers (Table 4). On multivariate analysis, having more than two smokers in the household, being in the same year in school as the index patients, and having received bad news in the preceding 3 months remained associated with meningococcal carriage (Table 5).

 

Table 3. Risk factors for meningococcal carriage in a Welsh secondary school
						Exposed		Nonexposed
	Exposeda		Nonexposed
							B15		B15
	Meningo-		Meningo-		Odds	B15	P1.16	B15	P1.16	Odds
	coccal	Non-	coccal	Non-	ratio	P1.16	non-	P1.16	non-	ratio
Variable	carrier	carrier	carrier	carrier	(95% CI)	carrier	carrier	carrier	carrier	(95% CI)
Year 11a	33	96	20	477	8.20b	11	118	0	497	Undefb
					(4.34-15.56)
Same classes	10	42	43	530	2.93b	1	121	10	494	0.41
as index casesc					(1.28-6.58)					(0.02-3.13)
Smoker	21	136	32	437	2.11b	3	154	8	461	1.12
					(1.12-3.94)					(0.23-4.71)
Other smoker	26	202	27	371	1.77b	4	224	7	391	1.00
in household					(0.99-3.24)					(0.24-3.84)
Student smoker and	12	70	41	503	2.10b	2	80	9	535	1.49
other in household					(1.00-4.41)					(0.00-7.54)
>2 smokers in	9	37	44	535	2.96b	1	45	10	567	1.26
householdc					(1.24-6.89)					(0.00-12.81)
Football teamc	6	88	47	415	0.60	3	91	8	454	1.87
					(0.22-1.54)					(0.38-8.02)
Rugby teamc	3	29	50	466	0.96	1	31	10	506	1.63
					(0.22-3.51)					(0.00-13.27)
Hockey teamc	3	29	50	467	0.97	1	31	10	507	1.64
					(0.22-3.52)					(0.00-13.30)
Netball teamc	1	54	52	452	0.16	0	55	11	493	0.00
					(0.01-1.13)					(0.00-4.46)
Any sport	10	172	43	401	0.54	3	179	8	436	0.91
					(0.25-1.16)					(0.19-3.83)
Regular youth	21	180	32	341	1.24	3	198	8	365	0.69
clubc					(0.67-2.31)					(0.14-2.93)
Regular discob	30	279	23	248	1.16	4	305	7	264	0.49
					(0.63-2.14)					(0.12-1.92)
Attendance at	23	111	29	461	3.29b,c	8	126	3	487	10.31b
partyc					(1.75-6.18)					(2.42-50.34)
Cubs/brownies/	1	42	52	531	0.24	0	43	11	572	0.00
scouts/guides					(0.01-1.72)					0.00-0.00
Life event	18	146	35	427	1.50	2	162	9	453	0.62
					(0.79-2.86)					(0.00-3.15)
Death in familyc	4	56	49	516	0.75	0	60	11	554	0.00
					(0.22-2.30)					(0.00-4.58)
Change of housec	5	33	48	539	1.70	0	38	11	576	0.00
					(0.55-4.89)					(0.00-7.63)
Received bad	15	79	38	493	2.46*	2	92	9	522	1.26
newsc					(1.22-4.91)					(0.00-6.46)
Travelc	6	107	47	464	0.55	1	112	10	501	0.45
					(0.21-1.40)					(0.02-3.48)
aSame school year as index case. bp < 0.05. cData missing.

 

Table 4. Medical factors associated with memingococcal carriage in a Welsh secondary school
						Exposed		Nonexposed
	Exposeda		Nonexposed
							B15		B15
	Meningo-		Meningo-		Odds	B15	P1.16	B15	P1.16	Odds
	coccal	Non-	coccal	Non-	ratio	P1.16	non-	P1.16	non-	ratio
Variable	carrier	carrier	carrier	carrier	(95% CI)	carrier	carrier	carrier	carrier	(95% CI)
Recent illness	43	482	10	91	0.81	7	518	4	97	0.33
					(0.37-1.80)					(0.08-1.37)
Recent injury	10	127	43	446	0.82	0	137	11	478	0.00
					(0.37-1.75)					(0.00-1.71)
History of	8	60	45	511	1.51	3	65	8	548	3.16
tonsillectomy/ adenoidectomya					(0.62-3.56)					(0.64-13.68)
Close contact	12	72	40	496	2.07b	3	81	8	528	2.44
with case of					(0.99-4.34)					(0.50-10.51)
meningococcal
diseasea
aData missing. bp < 0.05.

 

Table 5. Factors remaining significant for meningitidis carriage in final model
	Odds ratio	Odds ratio
	(95% CI)	(95% CI)
Variable	unadjusted	adjusteda
Year 11b	8.20	8.61
	(4.34-15.56)	(4.66-15.91)
>2 smokers in	2.96	2.99
household	(1.24-6.89)	(1.25-7.15)
Received bad news	2.46	2.67
	(1.22-4.91)	(1.32-5.40)
aadjusted for other significant variables.
bsame school year as index case.

For carriage of the epidemic strain, N. meningitidis B15 P1.16, four factors were associated: being in year 11, being older than 14, having attended the end-of-year party, and being male. Because carriage of the epidemic strain was confined to year 11 students (who were >14 years of age), multivariate analysis was not performed. Within year 11, no single factor was associated with carriage of N. meningitidis B15 P1.16.

Conclusions

In February 1995, we investigated risk factors for the carriage of any meningococci among the contacts of three ill students at another Welsh secondary school (8). These index patients were students in different school years, and 2 (1.7%) of 119 contacts carried the epidemic strain (type B2b P1.10). In the current outbreak, we identified 11 (1.5%) of 744 students with the epidemic strain (type B15 P1.16). In contrast, outbreaks of disease associated with serogroup C disease are typically accompanied by lower rates of carriage in populations at risk. However, outbreaks of group C disease involving higher carriage rates are occasionally described. In an outbreak at an agricultural college in England, carriage of the epidemic strain of serogroup C organisms among students and staff was 6.2% (9). In the current outbreak, the fact that all carriers of the epidemic strain were in the same school year as the two index patients enabled us to examine risk factors for carriage of the epidemic strain. Risk factors for the carriage of any meningococci may differ. For example, in an outbreak of six cases among first-year students at Southampton University (United Kingdom) in 1997, 0.9% of students surveyed carried serogroup C strains; however, no first year students were carriers (10).

Better knowledge of risk factors for carriage of epidemic meningococci may help identify close contacts who are candidates for antimicrobial therapy to eliminate nasal carriage and prevent spread of disease (11). Carriers of an epidemic strain with the potential to infect others may be missed, and a number of people may receive unnecessary antibiotics, which has implications for the spread of antibiotic resistance.

Carriage of any meningococci was associated in the univariate analysis with the well-described risk factors of increasing age and smoking (active and passive) (12-14). Smoking may predispose to colonization by inhibiting bronchial ciliary action (12). We also found increasing age and active smoking to be associated with carriage in our previous study (8). In the current study, receipt of bad news was associated. No obvious biological mechanism exists to explain what may be a chance finding, although recent stress has been described as a risk factor for meningococcal disease (6). Being in the same year as the index patients and attending the end-of-year party were risk factors for carriage of any strain of meningococci in this outbreak, mainly because these were the only two risk factors associated with carriage of the epidemic strain. These two factors reflect the kinds of social contacts among teenagers and young adults that may permit spread of meningococci. In a review of 22 school-based clusters between 1989 and 1993, the patients in nine of the clusters had contact through extracurricular activities; these activities in four clusters were parties or dances (15). Patronage of a particular bar was implicated in the university outbreak in Illinois (16), and a particular discotheque in an outbreak among eight adults (five of whom were teenagers) in Corrientes, Argentina (17). Such social settings differ from the residential settings, of outbreaks among military recruits and prisoners, where overcrowding and proximity of beds may permit transmission (18).

Attendance at the party may have been the critical factor in carriage of the epidemic strain among year 11 students. However, another hypothesis may account for our observations. Young adults who socialize frequently at discotheques and parties may, particularly if they smoke, be at higher risk for carriage of meningococci of all types. This increased long-term risk for disease may have a protective effect against a virulent outbreak strain (19). In contrast, those who participate infrequently in social events such as the end-of-year party may be at higher risk. This hypothesis may explain some of the risk for first-year university students. In addition to longitudinal studies, combining the results of surveys during outbreaks may help provide a more scientific basis for the management of future outbreaks.

Dr. Fitzpatrick is a lecturer in the department of Public Health Medicine and Epidemiology, University College, Dublin, Ireland. Her areas of expertise and research interests include epidemiology of prostate cancer and infectious and chronic diseases and health services research.

Acknowledgment

The authors thank the Meningococcal Reference Unit, Manchester PHL, for further examination and serogrouping of isolates.

Address for correspondence: Roland L. Salmon, PHLS Communicable Disease Surveillance Centre (Wales), Abton House, Wedal Rd, Roath, Cardiff, CF4 3QX, United Kingdom; fax: 44-1222-521-987; e-mail: roland.salmon@phls.wales.nhs.uk

References

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