Concurrent Infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in Children during a Cryptosporidiosis Outbreak in a Pediatric Hospital in China

Yaoyu Feng,Meijin Guo,Lihua Xiao,Lili Liu,Liping Duan,Jianbin Ye,Lin Wang,Yaqiong Guo

doi:10.1371/journal.pntd.0002437

Abstract

BackgroundOver 200 cryptosporidiosis outbreaks have been reported, but little is known if other enteric pathogens were also involved in some of these outbreaks. Recently, an outbreak of cryptosporidiosis linked to poor hygiene by two Cryptosporidium hominis subtypes occurred in a pediatric hospital ward (Ward A) in China, lasting for more than 14 months. In this study, the concurrence during the outbreak of three other enteric pathogens with a similar transmission route, Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile, was assessed.Methods/Principal FindingsThe occurrence of G. duodenalis, E. bieneusi, and C. difficile in 78 inpatients from Ward A and 283 and 216 inpatients from two control wards (Wards C and D) in the same hospital was examined using molecular diagnostic tools. Significantly higher infection rates were found in children in Ward A for all study pathogens than in Wards C and D (P<0.01): 9.5% versus 1.4% and 0% for G. duodenalis, 10.8% versus 2.8% and 3.7% for E. bieneusi, and 60.8% versus 37.8% and 27.8% for C. difficile, respectively. These differences were mostly seen in children ≤12 months. Enteric pathogen-positive children in Ward A (31/58 or 53.4%) were more likely to have mixed infections than those in Ward C (4/119 or 3.4%) or D (5/68, 7.4%; P<0.01). Having cryptosporidiosis was a risk factor for G. duodenalis (OR = 4.3; P = 0.08), E. bieneusi (OR = 3.1; P = 0.04), and C. difficile (OR = 4.7; P<0.01) infection. In addition, a lower diversity of G. duodenalis, E. bieneusi, and C. difficile genotypes/subtypes was observed in Ward A.Conclusions/SignificanceData from this study suggest that multiple pathogens were concurrently present during the previous cryptosporidiosis outbreak. Examination of multiple enteric pathogens should be conducted when poor hygiene is the likely cause of outbreaks of diarrhea.

Highlights

Cryptosporidium is a significant cause of diarrhea in humans worldwide [1]
The transmission of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile is poorly understood in developing countries despite their wide occurrence. Because they are transmitted by the same fecal-oral route as Cryptosporidium, in this study, we have examined the occurrence of these enteric pathogens in children during a cryptosporidiosis outbreak in a pediatric hospital in China
Four parasites including Cryptosporidium, G. duodenalis, E. bieneusi and C. difficile were analyzed in this study and no examinations of bacteria or viruses were conducted

Summary

Introduction

Cryptosporidium is a significant cause of diarrhea in humans worldwide [1]. Humans can acquire Cryptosporidium infections through the fecal-oral route via direct person-to-person or animalto-person contact, or ingestion of contaminated water or food [2]. Similar to Cryptosporidium, pathogens like Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile are significant causes of diarrhea in humans worldwide and can be transmitted from persons to persons by the same fecal-oral route involved in cryptosporidiosis occurrence [1,5,6]. All of these pathogens are major causes of healthcare-associated infections, especially Clostridium difficile [7,8,9]. The concurrence during the outbreak of three other enteric pathogens with a similar transmission route, Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile, was assessed

Methods

Results

Conclusion