Respiratory pathogens among ill pilgrims and the potential benefit of using point-of-care rapid molecular diagnostic tools during the Hajj.

We investigated respiratory pathogens among ill Hajj pilgrims from Marseille. We also discuss the potential role of point-of-care (POC) rapid molecular diagnostic tools for this purpose. Clinical data were collected using a standardised questionnaire. Influenza A and B viruses, human rhinovirus and human coronaviruses, Staphylococcus aureus, Streptococcus pneumoniae, Haemophilus influenzae and Klebsiella pneumoniae were investigated using real-time PCR in respiratory samples obtained during travel, at the onset of symptoms. 207 participants were included. A cough, expectoration, rhinitis and a sore throat were the most frequent respiratory symptoms, followed by loss of voice and dyspnoea. 38.7% and 25.1% of pilgrims reported a fever and influenza-like symptoms, respectively. 59.4% pilgrims received antibiotics. Rhinovirus (40.6%) was the most frequent pathogen, followed by S. aureus (35.8%) and H. influenzae (30.4%). Virus and bacteria co-infections were identified in 28.5% of participants. 25.1% pilgrims who were positive for respiratory bacteria did not receive antibiotic treatment. In the context of the Hajj pilgrimage, it is important to detect infections that can be easily managed with appropriate treatment, and those that can affect prognosis, requiring hospitalisation. POC rapid molecular diagnostic tools could be used for patient management at small Hajj medical missions and to rationalise antibiotic consumption among Hajj pilgrims.

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.

Acquisition of multidrug-resistant bacteria and colistin resistance genes in French medical students on internships abroad.

BACKGROUND: Acquisition of multidrug resistant bacteria (MDR) and colistin resistance genes by international travellers has been demonstrated. Studies conducted in medical students during internships abroad are scant. METHODS: Nasopharyngeal, rectal, and vaginal swabs samples were collected from 382 French medical students before and after travel to investigate the acquisition of MDR bacteria. The bacterial diversity in the samples was assessed by culture on selective media. We also genetically characterised the isolates of MDR bacteria including Extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E), methicillin-resistant Staphylococcus aureus (MRSA), and Carbapenemase-producing Enterobacteriacae (CPE) using the real-time polymerase chain reaction method. The samples were collected from 293 students and were investigated for mcr colistin-resistance genes using RT-PCR directly on the samples, followed by conventional PCR and sequencing. RESULTS: A proportion of 29.3% (112/382) of the participants had acquired ESBL-E and 2.6% (10/382) had acquired CPE. The most common species and ESBL-E encoding gene were Escherichia coli (125/127 isolates, 98.4%) and blaCTX-M-A (121/127, 95.3%), respectively. A proportion of 6.8% (20/293) of the participants had acquired mcr-1 genes, followed by mcr-3 (1/293, 0.3%) and mcr-8 (1/293, 0.3%). We found that taking part in humanitarian missions to orphanages (aRR = 2.01, p < 0.0001), being in contact with children during travel (aRR = 1.78, p = 0.006), the primary destination of travel being Vietnam (aRR = 2.15, p < 0.0001) and north India (aRR = 2.41, p = 0.001), using antibiotics during travel (aRR = 1.77, p = 0.01), and studying in 2018 (aRR = 1.55, p = 0.03) were associated with the acquisition of ESBL-E. When the primary destination of travel was Vietnam (aRR = 2.74, p < 0.0001) and the year of study was 2018 (aRR = 1.93, p < 0.002), this was associated with acquisition of colistin resistance genes. CONCLUSION: Medical students are at a potential risk of acquiring ESBL-E, CPE and colistin resistance genes. A number of risk factors have been identified, which may be used to develop targeted preventive measures.

Risk factors for symptoms of infection and microbial carriage among French medical students abroad.

OBJECTIVES: To investigate symptoms of infections and their risk factors among French medical students undertaking an internship abroad. METHODS: Clinical follow up, and qPCR-based respiratory, gastrointestinal, and vaginal pathogen carriages were prospectively assessed pre-travel and post-travel, in a cohort of medical students departing from Marseille, France. RESULTS: 293 students were included. 63.5%, 35.8%, and 3.6% of students reported gastrointestinal, respiratory, and vaginal symptoms, respectively. The acquisition rate of Enteroaggregative Escherichia coli and Enteropathogenic E. coli was 40.9% and 18.6%, respectively. A significant increase was observed for rhinovirus and Streptococcus pneumoniae by comparing the prevalence of pathogens in pre-travel and post-travel samples. Gardnerella vaginalis and Atopobium vaginae acquisition rates were 12.9% and 13.9%, respectively. Being female, primarily traveling to Vietnam, and living in basic accommodation conditions were independent risk factors for reporting respiratory symptoms. Students reporting respiratory symptoms were three times more likely to acquire S. pneumoniae. Traveling primarily to north India and Senegal were independent risk factors for diarrhea. CONCLUSION: This study makes it possible to identify the leading infectious diseases linked to travel in a group of French medical students undertaking an internship abroad and the risk factors on which to base targeting students for reinforced pre-travel advice.

Infectious disease symptoms and microbial carriage among French medical students travelling abroad: A prospective study.

BACKGROUND: In France, no previous studies have focused specifically on health problems among medical students during internships abroad including the clinical symptoms suggestive of infectious diseases and the acquisition of pathogen carriage. METHODS: Clinical follow up and qPCR based respiratory, gastrointestinal and vaginal pathogen carriage before and after travel were prospectively assessed in a cohort of medical students departing from Marseille, France. RESULTS: 134 students were included. 73.9%, 38.8% and 5.0% of students reported gastrointestinal, respiratory and vaginal symptoms, respectively. The acquisition rate of Enteroaggregative Escherichia coli (EAEC) and Enteropathogenic E. coli (EPEC) was 53% and 41%, respectively. The acquisition of respiratory viruses was low but associated with persisting symptoms, while bacterial acquisition ranged from 3.3% for Streptococcus pyogenes to 15.0% for Haemophilus influenzae. Gardnerella vaginalis and Atopobium vaginae acquisition rates were 7.7% and 14.3% respectively. Five students (5.1%) had molecular quantification criteria for bacterial vaginosis on return. CONCLUSION: This preliminary study demonstrates that besides the known risk of gastrointestinal and respiratory infections and associated changes in intestinal and respiratory microbiota, medical students abroad may also experience changes in vaginal microbiota leading, in some cases, to clinical symptoms or the acquisition of bacterial vaginosis, which may be asymptomatic.

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 respiratory viruses and presence of respiratory symptoms in French pilgrims during the 2016 Hajj: A prospective cohort study.

BACKGROUND: Viral respiratory tract infections are frequent among Hajj pilgrims. However, it is still not known whether viruses are responsible for the symptoms observed in sick pilgrims or whether they only colonize sick and asymptomatic pilgrims. PATIENTS AND METHODS: A prospective cohort study was conducted among French Hajj pilgrims in 2016. Medical follow-up and systematic nasal swabbing were performed pre- and post-Hajj. Additional samples were obtained per-Hajj, at symptom onset in ill pilgrims. Viruses were identified using the BioFire FilmArray® Respiratory multiplex qualitative PCR panel. RESULTS: 109 pilgrims were included. 83.5% presented respiratory symptoms during Hajj and 39.5% were still symptomatic on return. 5.5% of pre-Hajj, 95.2% of per-Hajj (at symptom onset) and 46.5% of post-Hajj samples tested positive (p < 0.0001). Acquisition rates of rhinovirus/enterovirus, coronavirus 229E and influenza A virus were respectively 38.6%, 19.8% and 2.0%. Although rhinovirus/enterovirus, coronavirus 229E and influenza A clearance were respectively 70.6%, 71.4% and 100% on return, overall virus carriage proportion on return was 75.0% in pilgrims with influenza-like illness and 44.0% in those who have never experienced this symptoms or resolved it (OR = 4.05, 95% CI [1.02-16.02]). CONCLUSIONS: Viruses likely play some role in the pathogenesis of the respiratory tract infections at the Hajj. Point of care-rapid multiplex PCR assays are valuable diagnosis tools in this context when used at respiratory symptom onset or soon after.

Bacterial respiratory carriage in French Hajj pilgrims and the effect of pneumococcal vaccine and other individual preventive measures: A prospective cohort survey.

BACKGROUND: Viral respiratory tract infections are known to be common in Hajj pilgrims while the role of bacteria is less studied. METHODS: Clinical follow-up, adherence to preventive measures and PCR-based pharyngeal bacterial carriage pre- and post-Hajj, were assessed in a cohort of 119 French Hajj pilgrims. RESULTS: 55% had an indication for pneumococcal vaccination. Occurrence of respiratory symptoms was 76.5%, with cough (70.6%) and sore throat (44.5%) being the most frequent; fever was reported by 38.7% pilgrims and 42.0% took antibiotics. Respiratory symptoms, fever and antibiotic intake were significantly more frequent in pilgrims with indication for vaccination against pneumococcal infection. The prevalence of S. pneumoniae carriage (1.8% pre-, 9.8% post-Hajj), H. influenzae carriage (0.9%, 45.4%) and K. pneumoniae (2.8%, 9.8%) significantly increased post-Hajj. Pilgrims vaccinated with conjugate pneumococcal vaccine were seven time less likely to present S. pneumoniae carriage post-Hajj compared to those not vaccinated (3.2% vs. 18.0%, OR = 0.15; 95% CI [0.03-0.74], p = 0.02). CONCLUSIONS: Pilgrims at risk for pneumococcal disease are more likely to suffer from febrile respiratory symptoms at the Hajj despite being immunized against pneumococcal disease and despite lowered S. pneumoniae carriage and should be targeted for reinforced prevention against respiratory infections.

Acquisition of enteric pathogens by pilgrims during the 2016 Hajj pilgrimage: A prospective cohort study.

BACKGROUND: Diarrhea can be frequent among Hajj pilgrims; however, data on its etiology are very limited. PATIENTS AND METHODS: A prospective cohort study was conducted among Hajj pilgrims in 2016. Medical follow-up and systematic rectal swabing were performed before leaving France and before leaving Saudi Arabia. Potential pathogens were identified using the BioFire FilmArray® Gastrointestinal multiplex qualitative PCR panel. RESULTS: 117 pilgrims were included and 13.7% experienced diarrhea during Hajj. Of the pre-Hajj samples, 32.5% were positive for at least one pathogen compared to 50% of post-Hajj samples (p = 0.0033). Diarrhea associated Escherichia coli strains, notably enteropathogenic E. coli (EPEC), enteroaggregative E. coli (EAEC), and Shiga-like toxin-producing E. coli, were acquired by 29.9%, 10.2%, and 6.5% pilgrims, respectively. Pilgrims with resolved diarrhea were significantly more likely to have post-Hajj EAEC positive samples, compared with those who did not suffer diarrhea (55.6% vs 16.5%). We found a lower prevalence of EPEC (22.5%) in pilgrims who declared washing their hands more frequently at the Hajj than usually as compared to others (40.0%). CONCLUSION: The acquisition of diarrhea associated E coli by Hajj pilgrims is of major concern given the high prevalence rate of third-generation cephalosporin-resistant E. coli in Saudi Arabia.

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.