Giardiasis: a diagnosis that should be considered regardless of the setting

Angel Escobedo

Giardiasis: a diagnosis that should be considered regardless of the setting

Epidemiology and Infection

Although Giardia, the aetiological agent of giardiasis, is one of the most prevalent intestinal parasitic infections world-wide, for industrialised countries, it is mainly appreciated as an imported disease with the minimal local transmission. However, the current evidence challenges this perception; Giardia has relevance beyond the high prevalence areas. This infection may be asymptomatic or cause gastrointestinal complains and long-term sequelae, including irritable bowel syndrome, chronic fatigue and impaired child growth and cognitive development. Its detection and diagnosis present a challenge to physicians who may not be familiar with this infection. To improve interventions to control this parasitosis, it is necessary to maintain a high index of suspicion and remain vigilant in finding cases at risk for infection. A better understanding of the characteristics of populations importing infections alongside improved methods to reliably classify infections as imported or acquired......Read more

Epidemiology and Infection cambridge.org/hyg Commentary Cite this article: Escobedo AA, Almirall P, Hanevik K, Cimerman S, Rodríguez-Morales AJ, Almanza C, Auza-Santivañez J (2018). Giardiasis: a diagnosis that should be considered regardless of the setting. Epidemiology and Infection 146, 1216–1218. https://doi.org/10.1017/S0950268818001504 Received: 13 February 2018 Revised: 9 May 2018 Accepted: 14 May 2018 First published online: 11 June 2018 Key words: Giardia; giardiasis; travel medicine Author for correspondence: Angel A. Escobedo, E-mail: escobedo@infomed.sld.cu © Cambridge University Press 2018 Giardiasis: a diagnosis that should be considered regardless of the setting Angel A. Escobedo 1,2 , Pedro Almirall 3 , Kurt Hanevik 4,5 , Sérgio Cimerman 6 , Alfonso J. Rodríguez-Morales 2,7 , Caridad Almanza 8 and Jhossmar Auza-Santivañez 9 1 Academic Paediatric Hospital ‘Pedro Borrás’ La Habana, Cuba; 2 Working Group on Zoonoses, International Society for Chemotherapy, Aberdeen, UK; 3 Municipal Centre of Hygiene, Epidemiology and Microbiology ‘Plaza’, La Habana, Cuba; 4 Norwegian National Advisory Unit on Tropical Infectious Diseases, Department of Medicine, Haukeland University Hospital, Bergen, Norway; 5 Department of Clinical Science, Faculty of Medicine, University of Bergen, Bergen, Norway; 6 Institute of Infectious Diseases ‘Emilio Ribas’, São Paulo, Brazil; 7 Research group Public Health and infection, Faculty of Health Sciences, Universidad Tecnológica de Pereira (UTP), Pereira, Risaralda, Colombia; 8 Central Clinic ‘Cira García’, La Habana, Cuba and 9 Academic Clinical and Surgical Hospital ‘Calixto García’, La Habana, Cuba Abstract Although Giardia, the aetiological agent of giardiasis, is one of the most prevalent intestinal parasitic infections world-wide, for industrialised countries, it is mainly appreciated as an imported disease with the minimal local transmission. However, the current evidence chal- lenges this perception; Giardia has relevance beyond the high prevalence areas. This infection may be asymptomatic or cause gastrointestinal complains and long-term sequelae, including irritable bowel syndrome, chronic fatigue and impaired child growth and cognitive develop- ment. Its detection and diagnosis present a challenge to physicians who may not be familiar with this infection. To improve interventions to control this parasitosis, it is necessary to maintain a high index of suspicion and remain vigilant in finding cases at risk for infection. A better understanding of the characteristics of populations importing infections alongside improved methods to reliably classify infections as imported or acquired locally will help to ensure early and accurate diagnosis. The evidence shows that public health problems like giar- diasis are global issues that need to be addressed collectively by both high and low prevalence countries. We welcome the paper by Currie et al.[1], in which they emphasise the need for significant improvements around Giardia selection criteria and testing algorithms in their country and at international level. Their work is a valuable example which alerts readers about the necessity of considering Giardia infection also in low-prevalence settings. Giardia is estimated to cause annually 184 million clinical cases [2] and an associated 171 100 (115 777–257 315) disability-adjusted life years [3]. In industrialised countries, where the incidence of human giardiasis, the disease that Giardia causes, decreased after improvements of sanitary infrastructures and safe drinking water, it is seen to be principally associated with travelling to – or immigration from – endemic areas. As highlighted by Currie et al. many reports are challenging this perception [4–12]. Indeed, this disease is being increasingly con- sidered as a re-emerging disease because of its recognised role in numerous outbreaks of diar- rhoeal diseases in daycare centres and also due to water-borne associated outbreaks [13]. In industrialised countries, there are also deprived communities and groups in the population exposed to suboptimal hygienic conditions, placing them at increased risk of diarrhoeal disease [5, 8, 9]. This facilitates human to human transmission and also allows travel-acquired Giardia to spread more easily within these countries, a mechanism termed introduced autochtonous transmission. The routes of transmission are responsible for a substantial proportion of both diagnosed and undiagnosed giardiasis cases. For instance, in Germany, of 273 inter- viewed cases of giardiasis, 131 (48%) of cases were not associated with travelling abroad [6]. Additionally, untreated drinking water has been identified as a risk factor for sporadic giardia- sis in New Zealand [14]. Swallowing water while swimming in pools, recreational fresh water contact, drinking treated tap water and eating lettuce had positive and independent associa- tions with infection in a case-control study carried out in residents who had not recently trav- elled outside the UK [4], pointing out the possibility that even treated tap water is a source of sporadic giardiasis. Recently, Adam et al. analysed data on all giardiasis outbreaks reported to the US Centres for Disease Control and Prevention for 1971–2011, describing and highlighting the ability of this protozoan to cause outbreaks through multiple transmission routes [11], including waterborne (74.8%), foodborne (15.7%), person-to-person (2.5%), animal contact https://doi.org/10.1017/S0950268818001504 Downloaded from https://www.cambridge.org/core. IP address: 34.204.175.69, on 01 Feb 2022 at 19:56:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.

(1.2%) and unknown (n = 14, 5.8%) transmission. Transmission from ill children to household contacts has also been documented in outbreak investigations [15] and sexual activity, mainly in men who have sex with men, which results in faecal–oral contact can lead to transmission of Giardia [16]. There are several factors hampering the rapid diagnosis of Giardia infection in industrialised countries. Firstly, as in devel- oping countries, a large proportion of infected people do not develop symptoms but may shed Giardia cysts for a period of time [17, 18]. Secondly, in individuals who do develop symptoms, detection depends on clinical experience, technical skills and on available diagnostic resources [19]. These may vary widely between and within countries. Giardiasis may, therefore, go undiagnosed or may be treated inappropriately by physicians who are unfamiliar with this disease. According to a few studies carried out in developed countries [20, 21], physicians who see Giardia-infected individuals often lack the experience and aware- ness of the disease. For example, the American College of Obstetricians and Gynecologists in collaboration with the Centres for Disease Control and Prevention made a survey of obstetrician-gynecologists on their clinical and epidemiologic knowledge of giardiasis in pregnancy [20]. Good general knowl- edge about diagnosis, transmission and prevention was found. However, difficulties concerning the best way to treat this parasitic infection during pregnancy were identified [20]. In a survey of US pediatricians evaluating their knowledge and perceptions on the treatment of giardiasis in children, only 10% indicated they would suspect parasites in a patient with diarrhoea lasting more than 1–2 weeks [21]. History and physical exam (83.9%) and dur- ation of diarrhoea (74.4%) were the main clinical aspects for parasitic-induced infection, with about one-third (36.2%) only taking into account the possibility of intestinal parasites when all other possible causes had been ruled out. Other studies have shown that a significant number of patients with giardiasis had encounters with health professionals without the diagnosis being considered, given the frequently observed delay between the onset of illness and diagnosis [22–25]. Surprisingly, in one study, 10% of patients reported receiving drugs, such as cipro- floxacin, which is ineffective against this protozoan [25]. The dis- covery of Giardia as the cause of a large waterborne outbreak in Bergen, Norway was delayed due to no history of travel abroad among the many patients seeking medical care for diarrhoeal dis- ease [24]. These scattered reports underline the need to enhance efforts to provide education among general practitioners and pediatricians to be aware of Giardia as a cause of indigenous cases of diarrhoea and on how best to diagnose and effectively treat them. Additionally, faecal specimens are often not routinely requested from persons with diarrhoeal illnesses [26, 27]. If Giardia is suspected, the right specimen and specific tests must be ordered and sent to a laboratory where adequate diagnostic tools and skills are available [28]. For laboratory diagnosis, a mor- phological determination by microscopy is the most commonly used method [29], which is simple and fast. Unfortunately, it is less sensitive, requires multiple sample examinations and concen- tration procedures and needs to be performed by well-trained technicians. Additionally, as it requires multiple clinic visits, it may be associated with high rates of diagnostic drop-out. In some industrialised countries, innovative modern technology has replaced microscopy as a routine diagnostic tool; i.e. the use of multiplex polymerase chain reaction assays for the detection of Giardia and other gastrointestinal protozoan pathogens (that could be simultaneously present) is particularly valuable. It assists in detecting the true prevalence of Giardia as well as earlier detec- tion of outbreaks if performed on a broader array of patients with diarrhoea. Finally, the awareness of the community is low. In one study caregivers of children with diarrhoea and more specifically per- sistent diarrhoea induced by Giardia showed that relatively low proportions of caregivers had heard of Giardia (36%) [30]. There are important reasons to pay attention to under- diagnosis of Giardia infection. In some cases, Giardia can cause severe clinical manifestations such as acute and chronic diarrhoea (the latter defined in case of episodes lasting more than 4 weeks) [31]. This infection may also be accompanied with or without malabsorption, abdominal cramps, nausea, vomiting, increased flatulence and weight loss [32]. Additionally, a range of extra- intestinal manifestations and long-term consequences have been identified and associated with this protozoan infection [33]. A controlled prospective study of a cohort of individuals who had confirmed Giardia infection during a waterborne outbreak found a significantly increased risk for post-infectious irritable bowel syndrome and chronic fatigue even 6 years after the infec- tion [34]. Of interest in both high and low prevalence settings, two recent studies have shown that early exposure to- or persistent Giardia infection during first 6 months of life, even if asymptom- atic, contribute to increased intestinal permeability and to stunted growth at 2 years of age [35, 36]. The changing perspectives of the incidence and prevalence of giardiasis in industrialised countries, where it is still relatively neglected and underappreciated by practicing clinicians and maybe by caregivers, need to be taken into account. Giardiasis may exceed the current prevalence estimates. An increased aware- ness for indigenous transmission is hoped for and as a result, indi- cations for Giardia testing would not be only done in returning travellers, nor considered only in a chronic diarrhoeal disease context. This might avoid delays in diagnosis. Currie et al. [1] study reminds us that there are multiple potential areas for improvement in laboratory testing algorithms and diagnostic awareness of giardiasis. The evidence shows that public health problems like giardiasis are a global issue that needs to be addressed collectively by industrialised and develop- ing countries. This protozoan disease, as well as other enteric parasites, should be considered more often in the differential diagnosis. It should be on the clinical, epidemiological and pub- lic health agenda, to be carefully addressed, for better decision- making in public health policies. It is especially important to keep in mind that, as in most infectious diseases, ‘what goes around, comes around’. References 1. Currie SL et al. (2017) Under-reporting giardiasis: time to consider the public health implications. Epidemiology and Infection 145, 3007–3011. 2. Pires SM et al. (2015) Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly trans- mitted through food. PLoS ONE 10, e0142927. 3. Kirk MD et al. (2015) World health organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Medicine 12, e1001921. 4. Stuart JM et al. (2003) Risk factors for sporadic giardiasis: a case-control study in southwestern England. Emerging Infectious Diseases 9, 229–233. 5. Snel SJ, Baker MG and Venugopal K (2009) The epidemiology of giar- diasis in New Zealand, 1997–2006. New Zealand Medical Journal 122, 62–75. Epidemiology and Infection 1217 https://doi.org/10.1017/S0950268818001504 Downloaded from https://www.cambridge.org/core. IP address: 34.204.175.69, on 01 Feb 2022 at 19:56:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.

Epidemiology and Infection cambridge.org/hyg Giardiasis: a diagnosis that should be considered regardless of the setting Angel A. Escobedo1,2, Pedro Almirall3, Kurt Hanevik4,5, Sérgio Cimerman6, Commentary Cite this article: Escobedo AA, Almirall P, Hanevik K, Cimerman S, Rodríguez-Morales AJ, Almanza C, Auza-Santivañez J (2018). Giardiasis: a diagnosis that should be considered regardless of the setting. Epidemiology and Infection 146, 1216–1218. https://doi.org/10.1017/S0950268818001504 Received: 13 February 2018 Revised: 9 May 2018 Accepted: 14 May 2018 First published online: 11 June 2018 Key words: Giardia; giardiasis; travel medicine Author for correspondence: Angel A. Escobedo, E-mail: escobedo@infomed.sld.cu © Cambridge University Press 2018 Alfonso J. Rodríguez-Morales2,7, Caridad Almanza8 and Jhossmar Auza-Santivañez9 1 Academic Paediatric Hospital ‘Pedro Borrás’ La Habana, Cuba; 2Working Group on Zoonoses, International Society for Chemotherapy, Aberdeen, UK; 3Municipal Centre of Hygiene, Epidemiology and Microbiology ‘Plaza’, La Habana, Cuba; 4Norwegian National Advisory Unit on Tropical Infectious Diseases, Department of Medicine, Haukeland University Hospital, Bergen, Norway; 5Department of Clinical Science, Faculty of Medicine, University of Bergen, Bergen, Norway; 6Institute of Infectious Diseases ‘Emilio Ribas’, São Paulo, Brazil; 7Research group Public Health and infection, Faculty of Health Sciences, Universidad Tecnológica de Pereira (UTP), Pereira, Risaralda, Colombia; 8Central Clinic ‘Cira García’, La Habana, Cuba and 9Academic Clinical and Surgical Hospital ‘Calixto García’, La Habana, Cuba Abstract Although Giardia, the aetiological agent of giardiasis, is one of the most prevalent intestinal parasitic infections world-wide, for industrialised countries, it is mainly appreciated as an imported disease with the minimal local transmission. However, the current evidence challenges this perception; Giardia has relevance beyond the high prevalence areas. This infection may be asymptomatic or cause gastrointestinal complains and long-term sequelae, including irritable bowel syndrome, chronic fatigue and impaired child growth and cognitive development. Its detection and diagnosis present a challenge to physicians who may not be familiar with this infection. To improve interventions to control this parasitosis, it is necessary to maintain a high index of suspicion and remain vigilant in finding cases at risk for infection. A better understanding of the characteristics of populations importing infections alongside improved methods to reliably classify infections as imported or acquired locally will help to ensure early and accurate diagnosis. The evidence shows that public health problems like giardiasis are global issues that need to be addressed collectively by both high and low prevalence countries. We welcome the paper by Currie et al. [1], in which they emphasise the need for significant improvements around Giardia selection criteria and testing algorithms in their country and at international level. Their work is a valuable example which alerts readers about the necessity of considering Giardia infection also in low-prevalence settings. Giardia is estimated to cause annually 184 million clinical cases [2] and an associated 171 100 (115 777–257 315) disability-adjusted life years [3]. In industrialised countries, where the incidence of human giardiasis, the disease that Giardia causes, decreased after improvements of sanitary infrastructures and safe drinking water, it is seen to be principally associated with travelling to – or immigration from – endemic areas. As highlighted by Currie et al. many reports are challenging this perception [4–12]. Indeed, this disease is being increasingly considered as a re-emerging disease because of its recognised role in numerous outbreaks of diarrhoeal diseases in daycare centres and also due to water-borne associated outbreaks [13]. In industrialised countries, there are also deprived communities and groups in the population exposed to suboptimal hygienic conditions, placing them at increased risk of diarrhoeal disease [5, 8, 9]. This facilitates human to human transmission and also allows travel-acquired Giardia to spread more easily within these countries, a mechanism termed introduced autochtonous transmission. The routes of transmission are responsible for a substantial proportion of both diagnosed and undiagnosed giardiasis cases. For instance, in Germany, of 273 interviewed cases of giardiasis, 131 (48%) of cases were not associated with travelling abroad [6]. Additionally, untreated drinking water has been identified as a risk factor for sporadic giardiasis in New Zealand [14]. Swallowing water while swimming in pools, recreational fresh water contact, drinking treated tap water and eating lettuce had positive and independent associations with infection in a case-control study carried out in residents who had not recently travelled outside the UK [4], pointing out the possibility that even treated tap water is a source of sporadic giardiasis. Recently, Adam et al. analysed data on all giardiasis outbreaks reported to the US Centres for Disease Control and Prevention for 1971–2011, describing and highlighting the ability of this protozoan to cause outbreaks through multiple transmission routes [11], including waterborne (74.8%), foodborne (15.7%), person-to-person (2.5%), animal contact Downloaded from https://www.cambridge.org/core. IP address: 34.204.175.69, on 01 Feb 2022 at 19:56:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268818001504 1217 Epidemiology and Infection (1.2%) and unknown (n = 14, 5.8%) transmission. Transmission from ill children to household contacts has also been documented in outbreak investigations [15] and sexual activity, mainly in men who have sex with men, which results in faecal–oral contact can lead to transmission of Giardia [16]. There are several factors hampering the rapid diagnosis of Giardia infection in industrialised countries. Firstly, as in developing countries, a large proportion of infected people do not develop symptoms but may shed Giardia cysts for a period of time [17, 18]. Secondly, in individuals who do develop symptoms, detection depends on clinical experience, technical skills and on available diagnostic resources [19]. These may vary widely between and within countries. Giardiasis may, therefore, go undiagnosed or may be treated inappropriately by physicians who are unfamiliar with this disease. According to a few studies carried out in developed countries [20, 21], physicians who see Giardia-infected individuals often lack the experience and awareness of the disease. For example, the American College of Obstetricians and Gynecologists in collaboration with the Centres for Disease Control and Prevention made a survey of obstetrician-gynecologists on their clinical and epidemiologic knowledge of giardiasis in pregnancy [20]. Good general knowledge about diagnosis, transmission and prevention was found. However, difficulties concerning the best way to treat this parasitic infection during pregnancy were identified [20]. In a survey of US pediatricians evaluating their knowledge and perceptions on the treatment of giardiasis in children, only 10% indicated they would suspect parasites in a patient with diarrhoea lasting more than 1–2 weeks [21]. History and physical exam (83.9%) and duration of diarrhoea (74.4%) were the main clinical aspects for parasitic-induced infection, with about one-third (36.2%) only taking into account the possibility of intestinal parasites when all other possible causes had been ruled out. Other studies have shown that a significant number of patients with giardiasis had encounters with health professionals without the diagnosis being considered, given the frequently observed delay between the onset of illness and diagnosis [22–25]. Surprisingly, in one study, 10% of patients reported receiving drugs, such as ciprofloxacin, which is ineffective against this protozoan [25]. The discovery of Giardia as the cause of a large waterborne outbreak in Bergen, Norway was delayed due to no history of travel abroad among the many patients seeking medical care for diarrhoeal disease [24]. These scattered reports underline the need to enhance efforts to provide education among general practitioners and pediatricians to be aware of Giardia as a cause of indigenous cases of diarrhoea and on how best to diagnose and effectively treat them. Additionally, faecal specimens are often not routinely requested from persons with diarrhoeal illnesses [26, 27]. If Giardia is suspected, the right specimen and specific tests must be ordered and sent to a laboratory where adequate diagnostic tools and skills are available [28]. For laboratory diagnosis, a morphological determination by microscopy is the most commonly used method [29], which is simple and fast. Unfortunately, it is less sensitive, requires multiple sample examinations and concentration procedures and needs to be performed by well-trained technicians. Additionally, as it requires multiple clinic visits, it may be associated with high rates of diagnostic drop-out. In some industrialised countries, innovative modern technology has replaced microscopy as a routine diagnostic tool; i.e. the use of multiplex polymerase chain reaction assays for the detection of Giardia and other gastrointestinal protozoan pathogens (that could be simultaneously present) is particularly valuable. It assists in detecting the true prevalence of Giardia as well as earlier detection of outbreaks if performed on a broader array of patients with diarrhoea. Finally, the awareness of the community is low. In one study caregivers of children with diarrhoea and more specifically persistent diarrhoea induced by Giardia showed that relatively low proportions of caregivers had heard of Giardia (36%) [30]. There are important reasons to pay attention to underdiagnosis of Giardia infection. In some cases, Giardia can cause severe clinical manifestations such as acute and chronic diarrhoea (the latter defined in case of episodes lasting more than 4 weeks) [31]. This infection may also be accompanied with or without malabsorption, abdominal cramps, nausea, vomiting, increased flatulence and weight loss [32]. Additionally, a range of extraintestinal manifestations and long-term consequences have been identified and associated with this protozoan infection [33]. A controlled prospective study of a cohort of individuals who had confirmed Giardia infection during a waterborne outbreak found a significantly increased risk for post-infectious irritable bowel syndrome and chronic fatigue even 6 years after the infection [34]. Of interest in both high and low prevalence settings, two recent studies have shown that early exposure to- or persistent Giardia infection during first 6 months of life, even if asymptomatic, contribute to increased intestinal permeability and to stunted growth at 2 years of age [35, 36]. The changing perspectives of the incidence and prevalence of giardiasis in industrialised countries, where it is still relatively neglected and underappreciated by practicing clinicians and maybe by caregivers, need to be taken into account. Giardiasis may exceed the current prevalence estimates. An increased awareness for indigenous transmission is hoped for and as a result, indications for Giardia testing would not be only done in returning travellers, nor considered only in a chronic diarrhoeal disease context. This might avoid delays in diagnosis. Currie et al. [1] study reminds us that there are multiple potential areas for improvement in laboratory testing algorithms and diagnostic awareness of giardiasis. The evidence shows that public health problems like giardiasis are a global issue that needs to be addressed collectively by industrialised and developing countries. This protozoan disease, as well as other enteric parasites, should be considered more often in the differential diagnosis. It should be on the clinical, epidemiological and public health agenda, to be carefully addressed, for better decisionmaking in public health policies. It is especially important to keep in mind that, as in most infectious diseases, ‘what goes around, comes around’. References 1. Currie SL et al. (2017) Under-reporting giardiasis: time to consider the public health implications. Epidemiology and Infection 145, 3007–3011. 2. Pires SM et al. (2015) Aetiology-specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food. PLoS ONE 10, e0142927. 3. Kirk MD et al. (2015) World health organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Medicine 12, e1001921. 4. Stuart JM et al. (2003) Risk factors for sporadic giardiasis: a case-control study in southwestern England. Emerging Infectious Diseases 9, 229–233. 5. Snel SJ, Baker MG and Venugopal K (2009) The epidemiology of giardiasis in New Zealand, 1997–2006. New Zealand Medical Journal 122, 62–75. Downloaded from https://www.cambridge.org/core. IP address: 34.204.175.69, on 01 Feb 2022 at 19:56:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268818001504 1218 6. Espelage W et al. (2010) Characteristics and risk factors for symptomatic Giardia lamblia infections in Germany. BMC Public Health 10, 41. 7. Júlio C et al. (2012) Prevalence and risk factors for Giardia duodenalis infection among children: a case study in Portugal. Parasites & Vectors 5, 22. 8. Yoder JS et al. (2012) Giardiasis surveillance–United States, 2009–2010. MMWR Surveillance Summaries 61, 13–23. 9. Barry MA et al. (2013) Childhood parasitic infections endemic to the United States. Pediatric Clinics of North America 60, 471–485. 10. Pardhan-Ali A et al. (2013) Community-level risk factors for notifiable gastrointestinal illness in the Northwest Territories, Canada, 1991–2008. BMC Public Health 13, 63. 11. Adam EA et al. (2016) Giardiasis outbreaks in the United States, 1971– 2011. Epidemiology and Infection 144, 2790–2801. 12. Waldram A et al. (2017) Prevalence of Giardia infection in households of Giardia cases and risk factors for household transmission. BMC Infectious Diseases 17, 486. 13. Thompson RC (2000) Giardiasis as a re-emerging infectious disease and its zoonotic potential. International Journal of Parasitology 30, 1259–1267. 14. Snel SJ et al. (2009) A tale of two parasites: the comparative epidemiology of cryptosporidiosis and giardiasis. Epidemiology and Infection 137, 1641–1650. 15. Katz DE et al. (2006) Prolonged outbreak of giardiasis with two modes of transmission. Epidemiology and Infection 134, 935–941. 16. Escobedo AA et al. (2014) Sexual transmission of giardiasis: a neglected route of spread? Acta Tropica 132, 106–111. 17. Rendtorff RC (1954) The experimental transmission of human intestinal protozoan parasites. II. Giardia lamblia cysts given in capsules. American Journal of Hygiene 59, 209–220. 18. Versloot CJ et al. (2018) Intestinal pathogen clearance in children with severe acute malnutrition is unrelated to inpatient morbidity. Clinical Nutrition ESPEN 24, 109–113. 19. Escobedo AA et al. (2018) Why are patients with giardiasis not treated earlier? Two sides of the same coin. Clinical Infectious Diseases. doi: 10.1093/cid/ciy122. 20. Krueger A, Schulkin J and Jones JL (2007) Survey of obstetriciangynecologists about giardiasis. Infectious Diseases in Obstetrics and Gynecology 2007, 21261. 21. Attias E et al. 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Halliez MC and Buret AG (2013) Extra-intestinal and long term consequences of Giardia duodenalis infections. World Journal of Gastroenterology 19, 8974–8985. 34. Hanevik K et al. (2014) Irritable bowel syndrome and chronic fatigue 6 years after Giardia infection: a controlled prospective cohort study. Clinical Infectious Diseases 59, 1394–1400. 35. Rogawski ET et al. (2017) Determinants and impact of Giardia infection in the first 2 years of life in the MAL-ED birth cohort. Journal of Pediatric Infectious Disease Society 6, 153–160. 36. Donowitz JR et al. (2016) A prospective longitudinal cohort to investigate the effects of early life giardiasis on growth and all cause diarrhea. Clinical Infectious Diseases 63, 792–797. Downloaded from https://www.cambridge.org/core. IP address: 34.204.175.69, on 01 Feb 2022 at 19:56:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268818001504

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Giardiasis: a diagnosis that should be considered regardless of the setting