Pharyngeal Colonization Dynamics of Haemophilus influenzae and Haemophilus haemolyticus in Healthy Adult Carriers

Deepa Mukundan; Zafer Ecevit; Mayuri Patel; Carl F. Marrs; Janet R. Gilsdorf

doi:10.1128/JCM.00492-07

DOI: 10.1128/JCM.00492-07

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FIG. 1.
Dendrogram (generated using BioNumerics software) of isolates from carrier A based on the unweighted pair-group method with arithmetic averages analysis of PFGE band patterns following digestion with SmaI (A) or EagI (B). Isolate labels are to the right of each band pattern; the first number on the left is the carrier number, followed in numerical order by the month, week, and day the sample was collected; each isolate from the same day was further designated by an uppercase letter. The PFGE genotypes shown are S1 to S6 in panel A and E7 to E11 in panel B.
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FIG. 2.
Dendrogram (generated using BioNumerics software) of carrier B isolates digested with SmaI (A) and EagI (B). See the legend to Fig. 1 for an explanation of the isolate labels.
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FIG. 3.
Dendrogram (generated using BioNumerics software) of carrier C isolates digested with SmaI. See the legend to Fig. 1 for an explanation of the isolate labels.
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FIG. 4.
Dendrogram (generated using BioNumerics software) of carrier D isolates digested with SmaI. See the legend to Fig. 1 for an explanation of the isolate labels.

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TABLE 1.

Distinguishing H. influenzae and H. haemolyticus isolates

Species	Porphyrin	Hemolysis	7F3 epitope of P6	iga
H. influenzae	Negative	Absent	Present	Present
H. haemolyticus	Negative	Present	Absent	Absent
Nonhemolytic H. haemolyticus	Negative	Absent	Absent	Absent
Variant	Negative	Absent	Present	Absent

TABLE 2.

Characteristics of the Haemophilus isolates from the four carriers

Characteristic	Value in carrier:				Total
Characteristic	A	B	C	D	Total
No. of isolates recovered	1,110	1,170	1,140	1,132	4,552
No. (%) porphyrin positive	889 (80)	543 (46)	984 (86)	956 (84)	3,372 (74)
No. (%) X and V factor dependent	76 (7)	559 (48)	98 (9)	127 (11)	860 (19)
No. encapsulated/total (%)	0/74	0/542	45/65 (69)	0/126	68/840 (8)
No. serotype b/total (%)	0/74	0/542	45/65 (69)	0/126	68/840 (8)
Hemolysis (total no. tested)	74	236	74	120	504
No. (%) positive	5 (7)	1 (0.42)	3 (4)	102 (85)	111/504 (22)
No. (%) negative	69 (93)	235 (99.6)	71 (96)	18 (15)	393/504 (78)
P6 epitope (total no. tested)	74	237	70	118	499
No. (%) positive	63 (85)	236 (99.6)	65 (93)	0	364/499 (73)
No. (%) negative	11 (15)	1 (0.42)	5 (7)	118 (100)	135/499 (27)
iga gene (total no. tested)	57	237	70	48	412
No. (%) positive	45 (79)	236 (99.6)	65 (93)	0	346/412 (84)
No. (%) negative	12 (21)	1 (0.4)	5 (7)	48 (100)	66/412 (16)
No. of H. influenzae isolates/total (%)	45/57 (79)	236/237 (99.6)	65/70 (93)	0/48 (0)	346/412 (84.0)
No. of H. haemophilus isolates/total (%)	5/57 (9)	1/237 (0.4)	3/70 (4)	38/48 (79)	47/412 (11.4)
No. of nonhemolytic H. haemophilus isolates/total (%)	6/57 (10)	0	2/70 (3)	10/48 (21)	18/412 (4.4)
No. of variant isolates (%)	1/57 (2)	0	0	0	1/412 (0.2)
No. of USS-PCR types	11 (n = 74)	16 (n = 541)	5 (n = 98)	12 (n = 125)
No. of PFGE genotypes	11 (n = 51)	15 (n = 205)	7 (n = 63)	10 (n = 39)

TABLE 3.
Distribution of unique PFGE genotypes as defined by digestion with SmaI (S1 to S6) or EagI (E7 to E11) restriction enzyme over time in carrier A
Day No. of isolates identified with genotype:
S1^a S2 S3 S4 S5 S6 E7^b E8 E9 E10 E11
0 1^c
1 2^c
2 1^e 1^e
3 7^c
8 1^e 2^c
14 2^c
15 1^c
16 1^c 1^c
17 1^c
22 1^c
23 1^c
60 1^c 2^d 1^c 1^d
64 1^c
71 1^c
81 3^c
108 2^c
116 1^c 2^d
122 1^c
128 2^c
141 4^c 1^c + 2^e
150 1^e
161 1^c
↵ a S genotypes based on digestion of genomic DNA with SmaI.
↵ b E genotypes based on failure to be digested with SmaI and successful digestion with EagI.
↵ c NTHI.
↵ d H. haemolyticus.
↵ e Nonhemolytic H. haemolyticus.
TABLE 4.
Distribution of unique PFGE genotypes as defined by digestion with SmaI (genotypes S1 to S11) or EagI (genotypes E12 to E15) restriction enzyme over time in carrier B
Day No. of isolates identified with genotype^a:
S1^b S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 E12^c E13 E14 E15
1 3
2 4
3 3
4 6
7 5
8 3 5
9 9 2
10 1 7
11 10 1
15 8 1
16 2
17 5 1
18 1 18
21 1
22 3 1 1
23 5 2
24 13 2
25 6
28 11
59 7 2
67 4 9
72 1 8 2
88 2
102 4
114 6
123 1 2 1 4
129 1 1 3 2 1
135 2
143 2
↵ a All isolates were confirmed to be NTHI.
↵ b S genotypes based on digestion of genomic DNA with SmaI.
↵ c E genotypes based on failure to be digested with SmaI and successful digestion with EagI.
TABLE 5.
Distribution of unique PFGE genotypes as defined by digestion with SmaI (S1 to S7) restriction enzyme over time in carrier C
Day No. of isolates identified with genotype:
S1^a S2 S3 S4 S5 S6 S7
0 1^b 1^b
1 2^b
2 2^b
3 1^b 1^b 1^d
4 3^b
8 1^c
11 2^b 1^b
15 2^b
16 1^b .
17 1^c
18 1^c
21 1^c
22 3^c
23 1^b 1^b 5^c
25 1^b 3^c
31 2^c
51 1^c
57 3^b 1^b
71 1^b 1^b 1^c
106 2^b
148 7^b 1^b
155 3^b 1^b
172 1^b 1^b
197 1^b
↵ a S genotypes based on digestion of genomic DNA with SmaI.
↵ b Capsule-deficient type b mutant.
↵ c NTHI.
↵ d Nonhemolytic H. haemolyticus.
TABLE 6.
Distribution of unique pulsed field gel electrophoresis (PFGE) genotypes as defined by digestion with SmaI (S1 to S10) restriction enzyme over time in Carrier D
Day No. of isolates identified with genotype:
S1^a S2 S3 S4 S5 S6 S7 S8 S9 S10
0 1^c 5^b
2 1^b 1^b 1^b 1^b
3 1^b
8 1^c
9 1^c
23 2^b 2^b
25 2^b
28 1^b
56 1^b
129 1^c
137 3^b
144 2^b
148 4^b 1^b
157 1^b
172 2^b 1^b
185 1^b
197 1^b 1^b
↵ a S genotypes based on digestion of genomic DNA with SmaI.
↵ b H. haemolyticus.
↵ c Nonhemolytic H. haemolyticus.

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Pharyngeal Colonization Dynamics of Haemophilus influenzae and Haemophilus haemolyticus in Healthy Adult Carriers

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Day	No. of isolates identified with genotype:
Day	S1^a	S2	S3	S4	S5	S6	E7^b	E8	E9	E10	E11
0										1^c
1										2^c
2							1^e	1^e
3										7^c
8		1^e							2^c
14	2^c
15	1^c
16	1^c					1^c
17	1^c
22						1^c
23	1^c
60	1^c			2^d						1^c	1^d
64	1^c
71										1^c
81	3^c
108	2^c
116	1^c				2^d
122	1^c
128	2^c
141	4^c		1^c + 2^e
150		1^e
161										1^c

Day	No. of isolates identified with genotype^a:
Day	S1^b	S2	S3	S4	S5	S6	S7	S8	S9	S10	S11	E12^c	E13	E14	E15
1				3
2											4
3											3
4				6
7											5
8			3	5
9				9										2
10		1		7
11				10										1
15				8			1
16				2
17				5				1
18			1	18
21				1
22	3	1			1
23				5											2
24													13		2
25													6
28													11
59												7	2
67												4	9
72					1							8	2
88												2
102												4
114												6
123					1	2				1		4
129				1	1	3			2	1
135									2
143									2

Day	No. of isolates identified with genotype:
Day	S1^a	S2	S3	S4	S5	S6	S7
0	1^b		1^b
1	2^b
2	2^b
3	1^b			1^b	1^d
4	3^b
8						1^c
11	2^b			1^b
15	2^b
16	1^b		.
17							1^c
18							1^c
21							1^c
22							3^c
23	1^b					1^b	5^c
25	1^b						3^c
31							2^c
51						1^c
57	3^b					1^b
71	1^b	1^b					1^c
106	2^b
148	7^b	1^b
155	3^b	1^b
172	1^b	1^b
197		1^b

Day	No. of isolates identified with genotype:
Day	S1^a	S2	S3	S4	S5	S6	S7	S8	S9	S10
0	1^c			5^b
2	1^b	1^b	1^b	1^b
3				1^b
8	1^c
9	1^c
23				2^b				2^b
25									2^b
28										1^b
56							1^b
129	1^c
137		3^b
144		2^b
148		4^b			1^b
157		1^b
172		2^b				1^b
185		1^b
197				1^b	1^b