Clostridioides difficile ribotypes 001 and 126 were predominant in Tehran healthcare settings from 2004 to 2018: a 14-year-long cross-sectional study

Figures & data

Table 1. Univariate and multivariate logistic regression predictors of CDI among studied patients.

Epidemiological characteristics	Univariate analysis	p-value	Multivariate analysis	p-value
	OR (95% CI)		OR (95% CI)
Children
<2	1.00		1.00
2–11	1.31 (0.55–3.07)	0.532	1.186 (0.49–2.84)	0.479
12–18	1.38 (0.54–3.51)	0.489	1.41 (0.54–3.71)	0.033
Adult
19–64	2.40 (1.10–5.22)	0.027	2.42 (1.07–5.47)	0.011
Elderly
65–74	2.94 (1.28–6.71)	0.010	3.06 (1.29–7.21)	0.029
75–84	2.68 (1.14–6.31)	0.023	2.68 (1.1.10–6.51)	0.001
≥85	4.37 (1.75–10.90)	0.002	4.70 (1.81–12.18)	0.701
Gender
Female	1.00		1.00
Male	0.876 (0.73–1.04)	0.145	0.897 (0.74–1.08)	0.255
Stool consistency
Watery	1.00		1.00
Loose	0.83 (0.69–1.01)	0.066	0.82 (0.67–0.99)	0.04
Mucous-filled	1.42 (0.29–6.8)	0.659	1.77 (0.33–9.3)	0.497
Formed	1.43 (0.82–2.49)	0.197	1.44 (0.81–2.5)	0.206
Medication exposure
Antimicrobials
Consumed	1.00		1.00
Not-consumed	1.03 (0.82–1.29)	0.780	0.87 (0.68–1.13)	0.317
Unknown	1.03 (0.78–1.36)		1.01 (0.75–1.35)	0.925
IBD drugs	1.00		1.00
Immunosuppressant	1.07 (0.44–2.60)	0.874	1.09 (0.44–2.72)	0.842
Corticosteroids	0.38 (0.15–0.94)	0.038	0.44 (0.17–1.12)	0.087
Anti-TNF	0.32 (0.38–2.70)	0.297	0.36 (0.42–3.09)	0.355
Corticosteroids + immunosuppressant	0.5 (0.17–1.46)	0.207	0.48 (0.16–1.46)	0.199
Corticosteroids + anti-inflammatory	0.41 (0.08–1.98)	0.270	0.34 (0.07–1.67)	0.187
Anti-inflammatory + immunosuppressant	0.77 (0.22–2.60)	0.678	0.72 (0.21–2.48)	0.613
Corticosteroids + anti-inflammatory + immunosuppressant	0.26 (0.03–2.17)	0.215	0.25 (0.03–2.11)	0.205
Chemotherapeutic agents	1.20 (0.37–3.85)	0.749	1.96 (0.53–7.24)	0.312
Duration of diarrhea
2–3 days	1.00		1.00
<1 day	0.80 (0.54–1.18)	0.263	0.80 (0.53–1.21)	0.305
1 day	0.85 (0.63–1.15)	0.302	0.88 (0.64–1.20)	0.434
>3 days	0.93 (0.77–1.14)	0.539	0.94 (0.76–1.15)	0.5599
Defecation (times/day)
3–5	1.00		1.00
1–2	1.34 (0.68–2.62)	0.388	1.29 (0.64–2.5)	0.471
5–8	1.12 (0.91–1.37)	0.260	1.11 (0.9–1.37)	0.312
8–10	1.38 (0.81–2.35)	0.229	1.55 (0.89–2.69)	0.114
>10	1.12 (0.85–1.48)	0.403	1.03 (0.83–1.38)	0.832
Comorbidities
Digestive system diseases	1.00		1.00
Respiratory system disease	0.96 (0.58–1.57)	0.876	1.13 (0.65–1.94)	0.658
Circulatory system disease	0.42 (0.51–1.65)	0.046	0.54 (0.22–1.22)	0.170
Genitourinary system disease	0.92 (0.51–1.65)	0.791	1.04 (0.54–2)	0.893
Endocrine disease	1.85 (1.14–3)	0.012	2.2 (1.32–3.99)	0.003
Blood cancer	0.59 (0.44–0.79)	0.001	1.07 (0.66–1.72)	0.772
Solid cancer	0.43 (0.1–1.83)	0.255	0.59 (0.13–2.63)	0.494
Immunodeficiency disorder	1.17 (0.58–2.37)	0.643	2.14 (0.97–4.68)	0.057
Neurological disorder	1 (0.65–1.55)	0.978	1.31 (0.78–2.19)	0.297
Skin disorder	4.95 (0.69–35.26)	0.110	12.8 (1.09–151.84)	0.043
Fever with unknown cause	0.75 (0.41–1.37)	0.359	0.80 (0.43–1.49)	0.489
Allergic disorder	4.95 (0.30–79.35)	0.258	5.88 (0.34–99.85)	0.220
Surgical procedure	1.55 (0.78–3.09)	0.206	1.95 (0.91–4.20)	0.085
Accident	2.47 (0.22–27.37)	0.460	4.93 (0.40–59.73)	0.210
Others	1.23 (0.56–2.70)	0.592	2.09 (0.84–5.16)	0.109
Hospital wards
Gastroenterology	1.00		1.00
Infectious disease	1 (0.71–1.4)	0.981	1.37 (0.92–2.04)	0.117
Internal	0.91 (0.68–1.2)	0.521	0.99 (0.72–1.38)	0.956
Surgery	1.12 (0.72–1.74)	0.586	1.00 (0.61–1.65)	0.975
Intensive care unit (ICU)	0.81 (0.55–1.19)	0.300	0.71 (0.45–1.14)	0.161
Pediatrics	0.86 (0.35 –2.09)	0.754	1.19 (0.43–3.33)	0.729
Oncology	0.73 (0.52–1.01)	0.064	0.88 (0.53–1.45)	0.621
Coronary care unit (CCU)	1.19 (0.54–2.62)	0.660	0.87 (0.37–2.05)	0.762
Urology	2.46 (0.73–8.2)	0.145	3.04 (0.84–11.03)	0.090
Gynecology	0.98 (0.43–2.24)	0.970	0.38 (0.38–2.19)	0.848
Endocrinology	1.89 (0.66–5.36)	0.230	1.35 (0.44–4.17)	0.596
Nephrology	0.91 (0.47–1.77)	0.798	0.78 (0.36–1.67)	0.528
Bone marrow transplant (BMT)	0.30 (0.16–0.55)	0.001	0.37 (0.17–0.79)	0.010
Orthopedics	0.82 (0.23–2.80)	0.752	0.41 (0.10–1.65)	0.211
Psychiatrics	3.93 (1.04–14.78)	0.042	3.47 (0.83–14.40)	0.086
Cardiology	1.03 (0.34–3.07)	0.949	1.11 (0.35–3.52)	0.853
General medicine	1.96 (0.37–10.21)	0.420	1.93 (0.35–10.48)	0.442
Out-patients	1.51 (1.09–2.08)	0.012	1.67 (1.19–2.33)	0.002
Laboratory tests
Leukocytosis	0.82 (0.65–1.04)	0.116	0.93 (0.72–1.21)	0.626
Neutropenia	0.64 (0.46–0.87)	0.006	0.89 (0.61–1.29)	0.551

CDI, Clostridioides difficile infection; IBD, inflammatory bowel disease; OR, odds ratio; CI, confidence interval. We first used the univariate analysis to select candidate variables (with p-value below 0.25) to perform multivariable logistic regression analysis. An OR with a 95% CI was calculated for all associations analyzed. Generally, statistical significance was declared for p-value less than 0.05 as shown in bold. Data were analyzed with ggplot2 and plotly R software packages.

Figure 1. Frequency of PCR ribotypes of 366 C. difficile isolates during the study period in Tehran. (A) Most commonly identified C. difficile PCR ribotypes. (B) Other C. difficile PCR ribotypes; ribotypes found at a frequency of less than 10 isolates in a year were grouped into the others category.

Figure 2. Distribution of C. difficile ribotypes during the study period (2004–2018). Each CE-ribotyping profile is represented by a different colour.

Figure 3. Distribution of C. difficile ribotypes according to patient age groups. (A) Distribution of PCR ribotypes of C. difficile isolates in children (<2–18 years). (B) Distribution of PCR ribotypes of C. difficile isolates in adults (19–64 years). (C) Distribution of PCR ribotypes of C. difficile isolates in elderly (65 to ≥85 years).

Table 2. Distribution of frequently found C. difficile RTs in HA-CDI and CA-CDI in inpatients and outpatients enrolled in this study.

C. difficile PCR RT	HA-CDI, n = 290 (%)	CA-CDI, n = 292 (%)
001	35 (12.1)	40 (13.7)
126	34 (11.7)	31 (10.6)
084	7 (2.4)	12 (4.1)
029	12 (4.1)*	3 (1.0)
038	4 (1.3)	11 (3.8)
266	10 (3.5)	5 (1.7)
002	8 (2.8)	5 (1.7)
003	6 (2.1)	7 (2.4)
014	6 (2.1)	7 (2.4)
070	9 (3.1)	4 (1.4)
Others	59 (20.3)	51 (17.5)
Unrecognized	62 (21.4)	85 (29.1)
Not typed	38 (13.1)	31 (10.6)

RT, ribotype; HA-CDI, healthcare-associated Clostridioides difficile infection; CA-CDI, community-associated Clostridioides difficile infection. RT 029 was significantly associated with HA-CDI (*p-value = 0.02).

Figure 4. Geographical distribution of C. difficile PCR ribotypes across different districts of Tehran. Pie charts represent the proportion of PCR ribotypes per 7 districts (D1–D4, D6, D7 and D11) of Tehran. The text on the map and in the centre of pie charts indicates the district number of typed isolates in Tehran. The percent of total numbers for the different ribotypes in the study districts are shown on each pie chart.

Figure 5. Relationship between prevalence of the most frequently found C. difficile PCR ribotypes in Tehran (RT 001, RT 126 and RT 084) and diversity of other ribotypes using Simpson’s reciprocal index. (A) Simpson’s reciprocal index of diversity for RT 001. (B) Simpson’s reciprocal index of diversity for RT 126. (C) Simpson’s reciprocal index of diversity for RT 084. (D) Simpson’s reciprocal index of RTs diversity with patient age.