Paragonimiasis: A knowledge and awareness survey of clinicians in southern Nigeria on a neglected tropical disease

Ekanem AM¹, Oloyede IP², Eduwem DU³

Abstract

Context: Paragonimiasis is one of the re-emerging neglected tropical diseases endemic in southern Nigeria. Its symptomology is similar to that of tuberculosis resulting in frequent cases of misdiagnosis

Objective: To determine the knowledge of clinicians in one of the endemic states in southern Nigeria on the cause and transmission of paragonimiasis.

Methods: A questionnaire based, descriptive cross-sectional study was conducted among Resident doctors in the departments of Internal medicine, Paediatrics, family medicine, community health and Obstetrics and gynaecology practising in University of Uyo Teaching Hospital. The doctors were consecutively recruited during their weekly academic training meetings in February 2020. Data was analysed using Stata version 10.

Results: A total of 61 respondents filled the questionnaires out of which 45 (73.8%) doctors admitted to have heard about the disease previously and the commonest source was from medical school in 29 (60.4%) of the respondents.  Forty five (73.4%) respondents correctly identified the causative agent of paragonimiasis as a helminth. The top three symptoms identified by respondents were haemoptysis 37 (60.7%), cough 37 (60.7%) and chest pain 30 (49.2%). Seventeen (27.9%) respondents could correctly identify the sequelae of paragonimiasis. The confirmatory investigations requested for were stool analysis, sputum analysis by six (28%) and five (23.8%) respondents respectively. Nineteen (31.1%) respondents knew the correct mode of transmission and 23 (37.7%) respondents knew that paragonimiasis mimics TB. Only 3 (15%) respondents knew praziquantel as drug of choice. The majority 43 (70.5%) had never treated the condition. Only 21 (34.4%) of the respondents had a good level of knowledge of the symptoms of paragonimiasis.

Conclusion: This study has identified a knowledge gap in the aetiology, route of transmission, diagnosis, treatment and complications of paragonimiasis among clinicians in an endemic area in southern Nigeria. We therefore recommend intensified efforts in training clinicians and other health workers on the aetiology and diagnosis of paragonimiasis through regular continuous medical education of their professional associations, departmental academic programs and update courses of the various postgraduate colleges in order to prevent misdiagnosis and delayed treatment of patients with paragonimiasis.

Keywords: Paragonimiasis, knowledge, clinicians, southern Nigeria.

Introduction

Paragonimiasis is one of the remerging neglected tropical diseases (NTD) being targeted for eradication by the World health organisation.¹ Reports from Southern Nigeria have confirmed its endemicity in this area.^2-6 A previous study has reported a prevalence of 4.9% among children in a water-adjoining/riverine community that shares a common boundary with Cameroon.⁷ Paragonimiasis is a food borne disease caused by the trematode Paragonimus, a lung fluke with about 10 species associated with morbidities in man. The commonest specie in man is P. westermani. Others include P. uterobilateralis and P. africanus, which are endemic in Africa.³ Human infection is acquired by the consumption of raw or partially cooked crustaceans (including crayfish and crabs).⁸ The pulmonary infection is characterized by cough, haemoptysis, chest pain and radiographic abnormalities, which are very similar to those seen in tuberculosis. The close similarities between paragonimiasis and tuberculosis both clinically and radiologically usually leads to a lot of misdiagnosis and confusion amongst clinicians.^9,10,11 As a result of frequent misdiagnosis, many patients end up having anti-tuberculous chemotherapy with a consequent delay in initiating the relevant treatment for paragonimiasis.^10,12 Shim and co-workers 13  reported that TB was diagnosed in 46% before the final diagnosis of pulmonary paragonimiasis was eventually made. Jeon et al¹⁴ reported that 30% of their patients had received a tentative diagnosis of pulmonary TB on their initial visit. Another diagnostic dilemma in adults is differentiating paragonimiasis from malignancies, even in areas where paragonimiasis is endemic.¹⁵ Twenty-eight percent of the pulmonary paragonimiasis patients in the series by Jeon et al¹⁴ were presumed to have had pulmonary malignancies on their initial visit. These results emphasize the necessity of generating awareness among clinicians about the inclusion of paragonimiasis in the differential diagnosis of TB, as well as pulmonary malignancies. These reports of delayed diagnosis and misdiagnosis are pointers to the emerging need for the parasitological training of doctors and other health workers as raised in some previous reports.^16,17
This study is therefore an attempt to determine the knowledge of the cause, transmission, diagnosis and treatment of paragonimiasis by clinicians in one of the endemic states in southern Nigeria. It is hoped that information from this study will assist in the design of interventions for the training of clinicians in paragonimiasis and TB endemic areas. It will also enable health policy makers to plan appropriate control measures subsequently.

Method

This descriptive questionnaire based cross-sectional study was conducted among medical doctors practising in Akwa Ibom State from January to February 2020. The study was carried out in Uyo, the capital city of Akwa Ibom state. The state is located in the south-south geopolitical zone of Nigeria. It has 31 Local Government Areas, 3 Senatorial Districts and a 2018 projected population of 5,737,270.¹⁸ There are a total of 220 Resident Doctors in University of Uyo Teaching hospital (UUTH). Majority of them are fulltime residents, however they are quite a number of supernumerary residents from the state government employ and some private facilities. The teaching hospital trains Resident Doctors in subspecialties of Community Health, Family Medicine, Internal Medicine, Paediatrics, Laboratory Medicine, Radiology, Dental Surgery, Ophthalmology, Otolaryngology, Obstetrics and Gynaecology and Surgery. Sub-specialties that are usually at the front line of seeing cases that may have paragonimiasis either in outpatient consultations or during outreaches include Community Health, Family Medicine, Internal Medicine, Paediatrics and Obstetrics and Gynaecology.
The study was conducted among the 113 frontline resident doctors practicing in UUTH. Resident Doctors in other departments were excluded from the study. The study period of January and February coincided with when most residents attend update courses with either the National Postgraduate Medical College of Nigeria or West African colleges as such some residents attended these courses. All residents in the five selected departments who consented were recruited into the study during their departmental academic meetings. Total sampling was thus used to recruit all available residents at the level of the departments. Consecutive sampling technique was used to recruit every consenting resident doctor at such meetings. Each department organizes weekly academic sessions as part of training for her resident doctors. Consent of the doctors were sought and all who agreed were recruited into the study by research assistants trained to collect data. Participants were asked not to complete the questionnaires if they had done so in previous meetings to avoid double recruitment of same participants
A self- administered semi structured pretested questionnaire developed by researchers based on the specific objectives of the study after a thorough literature review was used for data collection. It was pre-tested among NYSC doctors in the state and was further evaluated by experts in public health to ensure quality and content validity.
The questionnaire consisted of two sections (A and B). Section A obtained respondent's awareness and knowledge of causative agent, host, habitat, organs affected by paragonimiasis while section B obtained information on symptoms, diagnosis and treatment of paragonimiasis. In all, 20 questions assessed knowledge in these various areas. Every correct response was scored one point and wrong responses zero point. The maximum score per respondent was 20 points and minimum of zero point. The level of knowledge of paragonimiasis was categorized into poor (scores of less than 10) and good (scores of 10-20).
Data obtained was collated and analysed using Stata statistical software version 10.0 for windows. Categorical variables were summarised using frequencies and percentages.
Ethical clearance was obtained from the UUTH ethical committee. Informed consent was obtained from respondents. The voluntary nature of study was explained to them and non-participation attracted no penalties. They were assured of absolute confidentiality of data obtained from them.

Results

A total of 61 resident doctors responded to the questionnaires. The majority 57 (93.4%) were government employed doctors. About a quarter 15 (24.6%) were from obstetrics and gynaecology department. Twenty three (38.3%) doctors have spent between 6 to 10 years as doctors, while 22 (36.1%) doctors usually see patients /clients of all ages both males and females. (Table 1)
Forty five (73.8%) doctors had heard about the disease previously and the commonest source was from medical school in 29 (60.4%) of the respondents. The majority of doctors (73.8%) knew that helminths were the causative agent, however, only 8 (13.1%) knew that humans were the natural/definitive host. More than half of the doctors (37 out of 61) did not know the intermediate host. Twenty six (42.6%) doctors knew that the lungs was the natural habitat of the agent. The liver and brain were the other two organs known by the respondents as areas of affectation (32.8% and 19.7% respectively). (Table 2)
The two top symptoms known by the respondents were cough and haemoptysis 37(60.7%) respectively. Forty eight (78.7%) of the respondents did not know that paragonimiasis is endemic in Nigeria and almost an equal number 45(73.8%) did not know any other country where the disease is endemic. Thirty (49.2%) of the respondents knew the disease had sequelae; severe anaemia  and lung collapse  (23.5% and 17.6% respectively) were the top two sequelae mentioned by the respondents. (Table 3)
Only a few respondents knew the correct methods for confirming the diagnosis of paragonimiasis. The confirmatory investigations requested for were stool analysis, sputum analysis by six (28%) and five (23.8%) respondents respectively. Nineteen (31.1%) respondents knew the correct mode of transmission and 23 (37.7%) respondents knew that paragonimiasis mimics TB. Only 10 (16.4%) respondents knew that paragonimiasis could be diagnosed in their hospital. Only one (1.6%) respondent frequently requested for investigations to confirm paragonimiasis. The 2 top investigations requested by physicians were CXR and stool microscopy. (Table 4)
Twenty (32.8%) respondents knew that anti-helminthics are used for its treatment and only 3 (15%) respondents knew praziquantel as drug of choice. The majority 43 (70.5%) have never treated the condition. (Table 5)
Figure 1 shows that the level of knowledge of paragonimiasis among clinicians in southern Nigeria was generally low with 40 (65.6%) out of 61 respondents having poor knowledge of the aetiology, diagnosis, treatment and complications of paragonimiasis.

Discussion

Evidence of the re-emergence of paragonimiasis is reported in Nigeria 19 and other parts of the world.20 Knowledge of its symptoms among doctors is thus necessary for its prompt diagnosis and subsequent management of the condition. Our study has shown that 73.4% of our respondents were aware of the disease, however the level of knowledge of the diagnosis, treatment and complication of the disease is generally low. This is not unexpected as majority of those who had some knowledge reported that they were taught in medical school. Considering that most (70%)of our respondents  had been in practice for six years or more, it is therefore likely that they had forgotten most of what was taught and these may have accounted for the poor level of knowledge.
This study found that the majority of the respondents were aware of paragonimiasis. This finding is different from that of a similar study in Imo state which reported a lack of awareness of paragonimiasis amongst health workers in health centers.²¹ The higher proportion of respondents that have heard about the disease in this study may be due to the fact that respondents were doctors who had been taught and are supposed to be knowledgeable about the disease in order to be able to make accurate diagnosis of the condition. The Imo state study however, did not state the category of health workers. Low level of awareness of paragonimiasis (23.7%) was also reported among community members.²¹
Knowledge of symptoms of paragonimiasis is essential to making a correct diagnosis of the disease amongst health workers. This study revealed haemoptysis and cough as the two common symptoms known by the respondents while weight loss and fever were the least known symptom. Less than half of the doctors had good level of knowledge of the symptoms. In a related study, not even one case of paragonimiasis had been suspected or diagnosed in the health centers by the health workers despite the known fact of the re-emergence of the disease.²⁰ This low index of suspicion of paragonimiasis may keep the reemergence unnoticed and result in an increased misdiagnosis with TB. All cases of cough and haemoptysis or rusty sputum were investigated for pulmonary tuberculosis or HIV without the inclusion of paragonimiasis in the differential diagnosis.²⁰ A good level of knowledge of the symptoms of paragonimiasis which are shared with pulmonary tuberculosis is necessary for its diagnosis especially in areas where both diseases are endemic.
Our study showed that 73.8% of our respondents could identify the cause of paragonimiasis as a helminth, however only 31% of respondents knew that the disease was transmitted through eating improperly cooked crustaceans. This lack of knowledge of the route of transmission is likely to result in a deficient history, with an inability to make the proper diagnosis and give appropriate treatment. In addition, the doctor will be unable to appropriately counsel the client on the correct preventive measures to take to avoid reinfection. This lack of knowledge in the route of transmission of paragonimiasis may not be unconnected to the reduced hours of didactic training in human parasitology, the lack of well-qualified teaching staff in some universities which affects the quality of human Parasitology teaching and the compromised quality of laboratory teaching due to the ever increasing number of students, relatively restricted budgets, and limited laboratory facilities. In addition the reduced emphasis on parasite control may also contribute to the poor knowledge exhibited by our respondents. These factors have also been reported in Chinese study as some of the challenges faced in medical training in human parasitology.²²
The three highest confirmatory test indicated in our study population were stool, sputum and urine microscopy. Previous studies have reported the usefulness of stool microscopy in the detection of paragonimus spp especially in children who swallow their sputum.^23,24 Some of the demerits identified in stool microscopy were its poor sensitivity, low yield and the inability to differentiate paragonimus spp, from similar looking ova like clonorchis and schistosoma spp.²³ Therefore sputum microscopy is still found to be superior to stool microscopy in children.^25,26 However, a combination of stool and sputum microscopy could give a higher yield.²⁶
Two of our respondents reported that they occasionally requested for chest x-rays in their pursuit of the diagnosis of paragonimiasis. It should however be noted that some studies have reported the inability to differentiate paragonimiasis and tuberculosis radiologically.13,27 A study in southern Nigeria reported soft tissue wasting as the only differentiating radiographic feature between both diseases.⁹ The inability to differentiate TB and paragonimiasis has led to frequent misdiagnosis with many patients receiving Anti-tuberculous medication initially with a consequent delay in initiating the relevant treatment for paragonimiasis as has been reported in previous series.^10,12 Another diagnostic dilemma in adults is differentiating paragonimiasis from pulmonary malignancies, even in areas where paragonimiasis is endemic.¹⁵ Twenty-eight percent of the pulmonary paragonimiasis patients in a Korean series¹⁴ were presumed to have had pulmonary malignancies on their initial visit. These misdiagnosis is to be noted especially in southern Nigeria, where paragonimiasis and tuberculosis are endemic. In addition, paragonimiasis should also be considered as a differential for pulmonary malignancies. In view of the low level of knowledge of the aetiology, diagnosis, differential diagnosis and treatment of paragonimiasis among our resident doctors, we suggest that formal didactic trainings on paragonimiasis and other neglected tropical diseases should be incorporated into their residency training as this has been shown to improve their knowledge of parasitologic diseases in some residents in United States of America.²⁸

Conclusion
Our study has showed a low level of awareness among clinicians on the aetiology, route of transmission, diagnosis, and treatment of paragonimiasis. These results emphasize the necessity of generating awareness among clinicians about the inclusion of paragonimiasis in the differential diagnosis of TB, as well as pulmonary malignancies. We therefore recommend intensified efforts in training clinicians and other health workers on the aetiology and diagnosis of paragonimiasis through update courses in the various postgraduate colleges, continuous medical education of their various professional associations, and regular departmental seminars in order to prevent misdiagnosis and delayed treatment of patients with paragonimiasis.

References:

1. World health organization. Report on the Expert consultation to accelerate control of foodborne trematode infections, taeniasis and cysticercosis. WHO manila, Philippines December 2017: pp 1-31
2. Ibanga ES, Arene FO, Asor JE. Association of pulmonary paragonimiasis with active pulmonary tuberculosis in rural Yakurr community in Cross River basin. Mary Slessor J Med 2003;3:19-22.
3. Nwokolo C. Endemic Paragonimiasis in Africa.  Bull WHO 1974; 50: 569-71.
4. Ochigbo SO, Ekanem EE, Udo JJ. Prevalence and intensity of Paragonimus uterobilateralis infection among school children in Oban village, South Eastern Nigeria. Trop Doct 2007; 37: 224-26.
5. Iboh CI. Investigation of Crab-eating Influence on paragonimiasis infection in six communities of Abayong from Cross River State Nigeria. South Asian J Parasitol 2018; 1(1): 1-9.
6. Umoh NO, Useh MF. Epidemiology of paragonimiasis in Oban community of Cross River State, Nigeria. Mary Slessor J Med 2009;9(1):1-10.
7. Oloyede I, Ekanem E, Nyong E. Prevalence, co-prevalence and risk factors of pulmonary paragonimiasis and pulmonary tuberculosis in Nigerian children in the Niger delta area. East Afr Med J 2013; 90(6): 182-8.
8. Keiser J, Utzinger J. Emerging food-borne trematodiasis. Emerging Infect Dis 2005;11:1507-14.
9. Oloyede, I., Inah, G., Bassey, D., Ekanem, E. Comparative study of radiological findings in pulmonary paragonimiasis and tuberculosis in children in a Southern Nigeria fishing community. W Afr J Radiol 2014; 21 (1): 17-20
10. Lane MA, Barsanti MC, Santos CA, Yeung M, Lubner SJ, Weil GJ. Human Paragonimiasis in North America following Ingestion of Raw Crayfish. Clin Infect Dis 2009; 49:e55–61
11. Bidwell JL, Pachner RW. Hemoptysis: Diagnosis and management. Am Fam Physician 2005;72:1253-60.
12. Petborom P, Linasmita P, Kulpraneet M. Coinfection of Pulmonary Paragonimiasis and Pulmonary Tuberculosis in Thailand. J Med Assoc Thai 2016; 99 (8): S231-S236
13. Shim YS, Cho SY, Han HC. Pulmonary paragonimiasis: a Korean perspective. Semin Respir Med 1994;12:35-45.
14. Jeon K, Koh W-J, Kim H, et al. Clinical features of recently diagnosed pulmonary paragonimiasis in Korea. Chest 2005;128:1428-30.
15. Mukae H, Taniguka H, Matsumo N, et al. Clinicoradiologic features of pleuropulmonary paragonimus westermani on Kyusu Island, Japan. Chest 2001;120: 5111-20.
16. Song L-G, Zheng X-Y, Lin D-T, Wang G-X, Wu Z-D. Parasitology should not be abandoned: data from outpatient parasitological testing in Guangdong, China. Infect Dis Poverty 2017; 6:119 https://doi.org/10.1186/s40249-017-0332-0
17. Palmieri JR, Elswaifi SF, Fried KK. Emerging Need for Parasitology Education: Training to Identify and Diagnose Parasitic Infections. Am J Trop Med Hyg 2011; 84(6): 845–6
18. National Bureau of Statistics. Report on the 2018 Nutrition and Health Situation in Nigeria. June,2018
19. Eke RA, Enwereji EE. Re-Emergence of Paragonimiasis in Nigeria: A Case Report and Future Challenges. TAF Preventive Medicine Bulletin 2010; 9(6):703-706
20. Maruyama H, Noda S, Nawa Y. Emerging problems of parasitic disease in Southern Kyushu. Japan J Parasitol 1996; 45(3): 192–1200
21. Eke RA, Udochi I, Nwosu M, Enwereji EE, Emerole CV. Paragonimiasis Reemergence in Nigeria: Predisposing Factors and Recommendations for Early Intervention and Everlasting Eradication. ISRN Infect Dis 2013, Article ID 257810, 4 pages http://dx.doi.org/10.5402/2013/257810
22. Peng H-J, Zhang C, Wang C-M, Chen X-G. Current status and challenge of Human     Parasitology teaching in China. Pathogens and Global Health 2012; 106 (7): 386-390
23. Cho SY, Lee SH, Rim HJ, Seo BS. An evaluation of cellophane thick smear technique for mass stool examination. Korean J Parasitol 1969;7:48-52.
24. Rosenbaum SD, Reboli AC. Paragonimiasis. e-Medicine March 2006.
25. Upatham ES, Viyanant V, Kurathin GS, Vishari S, Brockelmann NY, Ardsuengnoen P. Paragonimus heterotremus infection in a community in a Suaburi province, Central Thailand. J Sci Soc Thailand 1995; 21: 1-9.
26. sMoyou-Somo R, Tagni-Zukam D. Paragonimiasis in Cameroon: Clinicoradiologic features and treatment outcome. Med Trop (Mars) 2003; 63: 163-67.
27. Singh TN, Karenbah S, Devi KS. Pleuropulmonary paragonimus mimicking pulmonary tuberculosis: a report of three cases. Indian J Microbiol 2005; 23: 131-34.
28. Bjorklund AB, Cook BA , Hendel-Paterson BR, Walker PF, Stauffer WM, Boulware DR. Impact of Global Health Residency Training on Medical Knowledge of Immigrant Health. Am. J. Trop. Med. Hyg. 2011; 85(3): 405–8