Acquisition of multidrug-resistant bacteria and encoding genes among French pilgrims during the 2017 and 2018 Hajj.

The objective of this study is to determine the acquisition of multidrug-resistant (MDR) bacteria and antibiotic resistance-encoding genes by French Hajj pilgrims and associated risk factors. Pilgrims traveling during the 2017 and 2018 Hajj were recruited. All pilgrims underwent two successive systematic nasopharyngeal and rectal swabs, pre- and post-Hajj. Specific culture media were used to screen for MDR bacteria, including methicillin-resistant Staphylococcus aureus (MRSA), carbapenem-resistant bacteria, and extended spectrum beta-lactamase producing Enterobacteriaceae (ESBL-E). qPCR was used to identify antibiotic resistance-encoding genes from cultured isolates. Direct screening of genes encoding for colistin resistance (mcr-1, 2, 3, 4, 5, and 8) from nasopharyngeal and rectal swabs was performed using qPCR, and positive qPCR results were simultaneously tested by sequencing. There were 268 pilgrims included. The percentage of pilgrims acquiring MDR bacteria during the Hajj was 19.4%. A total of 81 strains were isolated (1 carbapenem-resistant Acinetobacter baumannii, 12 MRSA, and 68 ESBL-E). ESBL-E strains were found in rectal samples of 6.0% pilgrims pre-Hajj and of 16.4% pilgrims post-Hajj. Only 0.4% pilgrims were positive for CARB post-Hajj and 1.9% carried nasal MRSA pre- and post-Hajj. In addition, 23 (8.6%) post-Hajj rectal swabs were positive for mcr genes (19 mcr-1 gene and 4 mcr-4 gene). No significant association was found between co-factors and acquisition of MDR bacteria or mcr genes. MDR bacteria and genes are acquired by pilgrims during the Hajj mass gathering. Rationalization of antibiotic consumption and implementation of measures to prevent transmission of bacteria among pilgrims during the event are of paramount importance.

Gastrointestinal symptoms and the acquisition of enteric pathogens in Hajj pilgrims: a 3-year prospective cohort study.

The acquisition of enteric pathogens and risk factors for Hajj-associated diarrhea in Hajj pilgrims is poorly documented. Pilgrims from Marseille participating in the Hajj in 2016-2018 underwent successive systematic rectal swabbing before and after their travel. Carriage of the main enteric pathogens was assessed by real-time PCR. Baseline demographics, adherence to individual preventive measures, gastrointestinal symptoms, and treatments were recorded. A total of 376 pilgrims were included. The median age was 62.0 years. During the Hajj, 18.6% presented at least one gastrointestinal symptom, 13.8% had diarrhea, and 36.4% had acquired at least one enteric pathogen. Enteropathogenic Escherichia coli (EPEC) and Enteroaggregative E. coli (EAEC) were the pathogens most frequently acquired by pilgrims (17.6% and 14.4%, respectively). Being female was associated with increased frequency of gastrointestinal symptoms during the pilgrimage (aOR = 2.38, p = 0.004). Enterohemorrhagic Escherichia coli (EHEC) acquisition was associated with a four-fold higher risk of reporting at least one gastrointestinal symptom and diarrhea (aOR = 3.68 and p = 0.01 and aOR = 3.96 and p = 0.01, respectively). Pilgrims who suffered from diarrhea were more likely to wash their hands more often (aOR = 2.07, p = 0.03) and to be either overweight (aOR = 2.71, p = 0.03) or obese (aOR = 2.51, p = 0.05). Enteric bacteria such as E. coli that are frequently associated with traveler's diarrhea due to the consumption of contaminated food and drink were frequently found in pilgrims. Respecting strict measures regarding food and water quality during the Hajj and adherence to preventive measures such as good personal hygiene and environmental management will help reduce the burden of gastrointestinal infections at the event.

Dynamics and genetic diversity of Haemophilus influenzae carriage among French pilgrims during the 2018 Hajj: A prospective cohort survey.

BACKGROUND: To investigate the genetic diversity of Haemophilus influenzae positive samples among French pilgrims attending the 2018 Hajj pilgrimage. METHOD: After screening by qPCR, multilocus sequence typing was performed for all H. influenzae-positive samples. The following housekeeping genes were amplified and assigned: adk, atpG, frdB, fucK, mdh, pgi and recA. RESULTS: 121 pilgrims were included. H. influenzae was positive in 35.5% pre-Hajj samples, 12.4% at day five post-arrival, 15.7% at day 12 post-arrival, and 43.0% post-Hajj. Of the 129 positive swabs for H. influenzae, only one sample at D12 was negative for all seven genes amplified by standard PCR. The adk, atpG, frdB, mdh, pgi, recA and fucK genes were positive in 123, 107, 122, 70, 127, 118 and 69 samples, respectively. One sequence of atpG and two of recA genes were not possible to assign. None of the sequences of fucK gene was successfully obtained. Consequently, a complete sequence type characterisation was not possible. Of the 128 obtained strains, 111 had distinct patterns of alleles. CONCLUSION: H. influenzae genotypes acquired were completely different from those present at pre-Hajj. We observed a great biodiversity and a lack of clonality of H. influenzae among French pilgrims during the 2018 Hajj. Further studies aiming at studying the genome of Hajj-acquired H. influenzae isolates are needed to define the clinical burden of H. influenzae infection during Hajj and to evaluate the potential interest of vaccination in Hajj pilgrims.

Environmental investigation of respiratory pathogens during the Hajj 2016 and 2018.

BACKGROUND: Respiratory tract infections are common in the context of the Hajj pilgrimage and respiratory pathogens can be transmitted via contact with contaminated surfaces. We sampled surfaces during the Hajj to detect the presence of respiratory bacteria and viruses. METHODS: Frequently touched surfaces at Mecca, Mina, Arafat and Medina were sampled. The common respiratory pathogens were tested by qPCR. RESULTS: 70/142 (49.3%) environmental samples collected were positive for at least one respiratory pathogen. Among the positive samples, Klebsiella pneumoniae was the bacterium most frequently tested positive (57.1%), followed by Streptococcus pneumoniae (12.9%), Staphylococcus aureus (10.0%) and Haemophilus influenzae (7.1%). 32.9% positive samples tested positive for rhinovirus and 1.4% for coronavirus. Surfaces with the highest rates of positive samples were kitchen tables (100%), water fountain faucet (73.3%) and edge of water coolers lid (84.6%). Samples collected in Mina were the most frequently contaminated with 68.8% being positive for at least one pathogen and 18.8% positive for a combination of multiple pathogens. CONCLUSION: These preliminary results indicate that respiratory pathogens are common in environmental surfaces from areas frequented by Hajj pilgrims. Further larger-scale studies are needed to better assess the possible role of environmental respiratory pathogens in respiratory infections in Hajj pilgrims.

Respiratory tract infections among French Hajj pilgrims from 2014 to 2017.

Respiratory tract infections (RTIs) are common among Hajj pilgrims, but risk factors for RTIs and respiratory pathogen acquisition during the Hajj are not clearly identified. Based on previous studies, most frequent pathogens acquired by Hajj pilgrims were investigated: rhinovirus, human coronaviruses, influenza viruses, Streptococcus pneumoniae, Staphylococcus aureus, Klebsiella pneumoniae and Haemophilus influenzae. 485 pilgrims were included. 82.1% presented with RTIs. Respiratory chronic diseases were associated with cough, Influenza-like illness (ILI) and the acquisition of H. influenzae. Vaccination against invasive pneumococcal diseases (IPD) and influenza was associated with a decrease in the acquisition of S. pneumoniae and prevalence of ILI (aRR = 0.53, 95%CI [0.39-0.73] and aRR = 0.69, 95%CI [0.52-0.92] respectively). Individuals carrying rhinovirus and H. influenzae-S. pneumoniae together were respectively twice and five times more likely to have respiratory symptoms. Individual with H. influenzae-K. pneumoniae carriage were twice (p = 0.04) as likely to develop a cough. The use of disposable handkerchiefs was associated with a decrease in the acquisition of S. aureus (aRR = 0.75, 95%CI [0.57-0.97]). Results could be used to identify pilgrims at increased risk of RTIs and acquisition of respiratory pathogens. Results also confirm the effectiveness of influenza and IPD vaccinations in reducing ILI symptoms and acquisition of S. pneumoniae carriage respectively.

The dynamics and interactions of respiratory pathogen carriage among French pilgrims during the 2018 Hajj.

We conducted this study to describe the dynamics of the acquisition of respiratory pathogens, their potential interactions and risk factors for possible lower respiratory tract infection symptoms (LRTI) among French pilgrims during the 2018 Hajj. Each participant underwent four successive systematic nasopharyngeal swabs before and during their stay in Saudi Arabia. Carriage of the main respiratory pathogens was assessed by PCR. 121 pilgrims were included and 93.4% reported respiratory symptoms during the study period. The acquisition of rhinovirus, coronaviruses and Staphylococcus aureus occurred soon after arrival in Saudi Arabia and rates decreased gradually after days 5 and 6. In contrast, Streptococcus pneumoniae and Klebsiella pneumoniae carriage increased progressively until the end of the stay in Saudi Arabia. Haemophilus influenzae and Moraxella catarrhalis carriage increased starting around days 12 and 13, following an initial clearance. Influenza viruses were rarely isolated. We observed an independent positive mutual association between S. aureus and rhinovirus carriage and between H. influenzae and M. catarrhalis carriage. Dual carriage of H. influenzae and M. catarrhalis was strongly associated with S. pneumoniae carriage (OR = 6.22). Finally, our model showed that M. catarrhalis carriage was negatively associated with K. pneumoniae carriage. Chronic respiratory disease was associated with symptoms of LRTI. K. pneumoniae, M. catarrhalis-S. aureus and H. influenzae-rhinovirus dual carriage was associated with LRTI symptoms. Our data suggest that RTIs at the Hajj are a result of complex interactions between a number of respiratory viruses and bacteria.

Antibiotic use for respiratory infections among Hajj pilgrims: A cohort survey and review of the literature.

BACKGROUND: To evaluate the occurrence and determinants associated with antibiotic use for respiratory tract infections (RTIs) among Hajj pilgrims. METHODS: Prospective cohort surveys were conducted among French pilgrims from 2012 to 2017. We also conducted a systematic review about available evidence for antibiotic consumption in relation with RTIs during the Hajj. RESULTS: 783 pilgrims were included in the survey. During the Hajj, 85.3% presented respiratory symptoms and 47.6% used antibiotics. Pilgrims with productive cough or fever were three times and twice as likely to have used antibiotics. Dry cough, sore throat and voice failure were also associated with increased antibiotic use. 26.3% of pilgrims presented symptoms compatible with a lower tract respiratory infection. According to the French recommendations, only 39.6% of pilgrims who used an antibiotic actually had an indication for it. Antibiotic intake was associated with an increased frequency of persistent symptoms post-Hajj (aRR = 1.31, 95%CI [1.04-1.66]). The review included 14 articles. The use of antibiotic for respiratory tract infections during the Hajj varied from 7% to 58.5%. In 9 studies, the antibiotic consumption rate was >30%. CONCLUSION: Respiratory tract infections are common during the Hajj, leading to high prevalence of inappropriate antibiotic intake.

Acquisition of a High Diversity of Bacteria during the Hajj Pilgrimage, Including Acinetobacter baumannii with blaOXA-72 and Escherichia coli with blaNDM-5 Carbapenemase Genes.

Pilgrims returning from the Hajj (pilgrimage to Mecca) can be carriers of multidrug-resistant bacteria (MDR). Pharyngeal and rectal swab samples were collected from 98 pilgrims before and after they traveled to the Hajj in 2014 to investigate the acquisition of MDR bacteria. The bacterial diversity in pharyngeal swab samples was assessed by culture with selective media. There was a significantly higher diversity of bacteria in samples collected after the return from the Hajj than in those collected before (P = 0.0008). Surprisingly, Acinetobacter baumannii strains were isolated from 16 pharyngeal swab samples (1 sample taken during the Hajj and 15 samples taken upon return) and 26 post-Hajj rectal swab samples, while none were isolated from samples taken before the Hajj. Testing of all samples by real-time PCR targeting blaOXA-51 gave positive results for only 1% of samples taken during the Hajj, 21/90 (23.3%) pharyngeal swab samples taken post-Hajj, and 35/90 (38.9%) rectal swab samples taken post-Hajj. One strain of A. baumannii isolated from the pharynx was resistant to imipenem and harbored a blaOXA-72 carbapenemase gene. Multilocus sequence typing analysis of 43 A. baumannii isolates revealed a huge diversity of 35 sequence types (STs), among which 18 were novel STs reported for the first time in this study. Moreover, we also found one Escherichia coli isolate, collected from a rectal swab sample from a pilgrim taken after the Hajj, which harbored blaNDM-5, blaCTX-M-15, blaTEM-1, and aadA2 (ST2659 and ST181). In conclusion, pilgrims are at a potential risk of acquiring and transmitting MDR Acinetobacter spp. and carbapenemase-producing Gram-negative bacteria during the Hajj season.

French Hajj pilgrims' experience with pneumococcal infection and vaccination: A knowledge, attitudes and practice (KAP) evaluation.

BACKGROUND: Transmission of respiratory infections poses a major public health challenge during the Hajj and Umrah in the Kingdom of Saudi Arabia. Acquisition of Streptococcus pneumoniae during Hajj has been studied in the past and recommendations for vaccination against S. pneumoniae have been made for high risk groups. METHODS: The purpose of this study was to assess the knowledge and attitudes of French Hajj pilgrims towards pneumococcal vaccination. Adult pilgrims departing from Marseille, France to Mecca for the 2014 Hajj season were administered a face-to-face questionnaire to ascertain their knowledge and attitudes towards pneumococcal vaccination before departing for Hajj. RESULTS: A total of 300 participants took part. Their overall knowledge about the severity of pneumonia and the existence of the vaccine was very low. Out of 101 participants who had an indication for pneumococcal vaccination, irrespective of their travel status, only 7% were advised to have the vaccine by their general practitioner. CONCLUSIONS: These results reinforce the need for better dissemination of information either before or during the pre-travel counselling. The visit to the travel clinic for receiving the mandatory meningococcal vaccination for Hajj is a good opportunity to update routine immunizations, including pneumococcal vaccination.

Acquisition of extended-spectrum cephalosporin- and colistin-resistant Salmonella enterica subsp. enterica serotype Newport by pilgrims during Hajj.

Gatherings like the Hajj involving many people who travel from different parts of the world represent a risk for the acquisition and dissemination of infectious diseases. In this study, acquisition of multidrug-resistant (MDR) Salmonella spp. in 2013 Hajj pilgrims from Marseille, France, was investigated. In total, 267 rectal swabs were collected from 129 participants before their departure and after their return from the pilgrimage as well as during the pilgrimage from patients with diarrhoea. Samples were screened for the presence of Salmonella using quantitative real-time PCR and culture. Whole-genome sequencing was performed to characterise one of the isolates, and the mechanism leading to colistin resistance was investigated. Six post-Hajj samples and one sample collected during a diarrhoea episode in Hajj were positive for Salmonella by real-time PCR, with five Salmonella enterica belonging to several serotypes recovered by culture, whereas no pre-Hajj sample was positive. Two of the isolates belonged to the epidemic Newport serotype, were resistant to cephalosporins, gentamicin and colistin, and harboured the bla(CTX-M-2) gene and a 12-nucleotide deletion in the pmrB gene leading to colistin resistance. This study shows that pilgrims acquired Salmonella bacteria, including a novel MDR clone, during the Hajj pilgrimage. This calls for more improved public health surveillance during Hajj because Salmonella is one of the most common diarrhoea-causing bacteria worldwide. Therefore, returning pilgrims could disseminate MDR bacteria worldwide upon returning to their home countries.

Foot ailments during Hajj: A short report.

A study of ailments of the feet in pilgrims of Hajj revealed that 31% of them suffered from blisters, and the prevalence was five times higher in females. The presence of comorbidity (diabetes, obesity and advanced age) warrants immediate attention to them to avoid serious complications.

Respiratory viruses and bacteria among pilgrims during the 2013 Hajj.

Pilgrims returning from the Hajj might contribute to international spreading of respiratory pathogens. Nasal and throat swab specimens were obtained from 129 pilgrims in 2013 before they departed from France and before they left Saudi Arabia, and tested by PCR for respiratory viruses and bacteria. Overall, 21.5% and 38.8% of pre-Hajj and post-Hajj specimens, respectively, were positive for ≥1 virus (p = 0.003). One third (29.8%) of the participants acquired ≥1 virus, particularly rhinovirus (14.0%), coronavirus E229 (12.4%), and influenza A(H3N2) virus (6.2%) while in Saudi Arabia. None of the participants were positive for the Middle East respiratory syndrome coronavirus. In addition, 50.0% and 62.0% of pre-Hajj and post-Hajj specimens, respectively, were positive for Streptococcus pneumoniae (p = 0.053). One third (36.3%) of the participants had acquired S. pneumoniae during their stay. Our results confirm high acquisition rates of rhinovirus and S. pneumoniae in pilgrims and highlight the acquisition of coronavirus E229.

Acquisition of Streptococcus pneumoniae carriage in pilgrims during the 2012 Hajj.

To investigate the nasal carriage of some respiratory bacterial pathogens that are responsible for infections associated with person-to-person transmission, we conducted a cohort survey of pilgrims departing to Mecca for the 2012 Hajj season. In this report, we demonstrate the acquisition of Streptococcus pneumoniae nasal carriage in returning Hajj pilgrims.

Circulation of respiratory viruses among pilgrims during the 2012 Hajj pilgrimage.

BACKGROUND: The Hajj is the oldest and largest annual mass gathering in the world and may increase the risk of spread of respiratory viruses. METHODS: We performed a prospective survey among a cohort of pilgrims departing from Marseille, France, to Mecca in the Kingdom of Saudi Arabia (KSA) for the 2012 Hajj season. Nasal swabs were collected from participants and tested for 11 respiratory viruses by real-time reverse transcription polymerase chain reaction. RESULTS: Of 165 participants sampled before departing to the KSA, 8 (4.8%) were positive for at least 1 virus (5 rhinovirus, 1 influenza C, 1 adenovirus, and 1 enterovirus). Seventy symptomatic pilgrims underwent additional nasal swabs during their pilgrimage in the KSA, of which 27 (38.6%) were positive for at least 1 virus (19 rhinovirus, 6 influenza A, 1 influenza C, 1 respiratory syncytial virus B, 1 metapneumovirus, 1 adenovirus, and 1 enterovirus). This was significantly higher than the 4.8% who were positive before departing for the KSA (P < .001). Of 154 pilgrims sampled before leaving the KSA, 17 (11%) were positive for at least 1 virus (13 rhinovirus, 3 adenovirus, 2 influenza B, and 1 enterovirus), which was also significantly higher than the percentage of positive pilgrims (4.8%), before departing for the KSA (P = .040). CONCLUSIONS: This study suggests a rapid acquisition of respiratory viruses among pilgrims during their stay in the KSA, most notably rhinovirus, and highlights the potential of spreading these infections in the pilgrims' home countries upon their return.