Paragonimiasis Reemergence in Nigeria: Predisposing Factors and Recommendations for Early Intervention and Everlasting Eradication

Effective paragonimiasis eradication programme in Nigeria eradicated the once endemic disease and no case was reported from 1980 to 2007.e �rst reported reemergence case was in 2007 and �vemore cases till January 2011 when this study was undertaken. is study is to determine the pre-disposing factors for the reemergence. e factors will help plan a sustainable long lasting and hopefully everlasting eradication programme. 2760 households from the identi�ed twelve villages with the endemic disease were systematically selected. Pretested questionnaires were interviewer administered to the head of each of the selected household. e data collected were analyzed quantitatively and qualitatively. e pre-disposing factors that precipitated the reemergence of the disease included low level of awareness of the disease by the entire populace including the healthworkers.is included the causative agent, the mode of transmission, and control; conservative cultural habits of preparing crab meal; eating improperly cooked crab and also insanitary disposal of faeces and sputum. A holistic eradication programme should be planned to have sustained activities that will usher in everlasting disease-free area. e programme should involve all people, policy makers, health workers, and the entire populace, taking care of peculiarities of the peoples habits.


Introduction
Reemergence of a disease came to limelight on the international scene when a bold attempt was made to eradicate malaria in Siri Lanka (then Ceylon) many decades ago [1].e resurgence of malaria hit the headlines in health fora at various times.Ever since various attempts have failed to produce lasting solutions aer an attempted eradication programme of many diseases.is paper focuses on reemergence of paragonimiasis, a lung-�uke, food-borne zoonotic disease spread across the world.Paragonimiasis occurs in East and South East Asia, West Africa, and Central and South America [2].e causative agent of this disease in man is Paragonimus metacercariae of 10 various identi�ed species.e species infecting man include P. uterobilateralis and P. africanus in Nigeria, West Africa.Other species infect man elsewhere in the world.e paragonimiasis agent goes through a circle of transmission from man or various crab eating carnivorous mammals like dogs to snails of several genera and then to fresh water crustacean as metacercariae infect crab eating carnivorous animals as their natural reservoir of the Paragonimus species.It is to be noted that species in any natural reservoir may infect any other natural reservoir as in the case of P. uterobilateralis which was formally known to be a parasite of dog in Cameroun and of mangoose and bush rats in Liberia but eventually became a parasite of man in Nigeria [3][4][5][6][7][8].
Reemergence of paragonimiasis in Japan and Nigeria had been well discussed in recent times.e picture of endemicity of paragonimiasis in Miyazaki-Prefecture, Japan, before 1950, had been well documented [9].Aer the 1950-1960 mass screening and prevention campaign by the Local Government, the disease drastically decreased.In the 1970s paragonimiasis was considered disease of the past in Miyazaki and other endemic areas in Japan.From late 1980s new case began to emerge sporadically in these previously endemic areas.e situation in Nigeria showed a similar trend of events.Endmicity of the disease was recorded as from 1964 [5][6][7][8]10].Civil war in Nigeria (1968)(1969)(1970) which caused a collapse in socioeconomic indices helped to make the disease a public health concern with very many cases of the disease in Nigeria.Following well-planned efficient and effective programme at the end of the war in Nigeria the disease was reported to be eradicated by 1980.No case of paragonimiasis for treatment was reported from 1980 to September 2007.However, reemergence of the disease was reported in October 2007 [10].Since 2007 to date this scenario of reemergence in Nigeria is like that reported in Japan.If nothing is done in Nigeria the disease reemergence will become a serious public health problem.
ere is therefore a great need to initiate this study to determine pre-disposing factors that precipiated the reemergence of the disease in Nigeria.It is noted that the recommendations to be made here, will help the policy makers and health workers plan efficient and effective eradication programme that will usher in everlasting eradication of the disease.e experience gained here will help policy makers and the health worker to successfully treat disease reemergence anywhere in the world.e program should take into consideration the society's peculiarities in the factors identi�ed.

Methodology
A cross-sectional study was carried out in the twelve villages along Imo, River Bank in Onu Imo Local Government Area of Imo State, Nigeria.ese villages are in the endemic areas of paragonimiasis.e River Bank is the breeding place of crabs infested with metacercariae of Paragonimus uterobilateralis.
A sampling frame of each of the twelve villages was made by enumerating all the households within the villages.A population of 2760 households was recorded.A sample size of 400 households was calculated using Lutz' formula of    2  2 .T 3: Identi�ed cultural methods for preparing crab meal (  ).

Methods
Frequency Percent Roasting/drying crab 344 86% Boiling and grinding crab as soup ingredient 400 100% Eating crab raw with alcohol 400 100% Selection of the 400 households out of the population of 2760 was by systematic sampling method using a sampling interval of seven.Data were collected from household interview using the questionnaire and review of health facilities record books.e reliability and validity of the questionnaire were ensured through vetting committee of health experts and also through a pretest of the questionnaire.
A total of 400 copies of the questionnaire was interviewer administered.An interactive discussion with the health providers at the health center was held in order to ascertain their level of awareness about paragonimiasis: index of suspicion and laboratory diagnosis of the disease.Data collected were analyzed quantitatively and qualitatively.Permission to carry out the survey was sought and obtained from the village heads and also from the individual respondents before administering the questionnaire on them.Data collected were handled in strict con�dence.

Result
Table 1 shows that age was statistically signi�cant in in�uencing knowledge and awareness of paragonimiasis among respondents (  ).About 23.75% respondents were aware of the disease.However no body was aware of paragonimiasis amongst the younger age group 25-35 years.Generally, younger age groups (25-46 years) were more ignorant about paragonimiasis in Nigeria than the elderly age group (47 years above).About 100% of respondents indicated that cultural acceptability of crabs as the people's delicacy was the strongest driving force for eating crabs, while ready availability of crabs in surrounding bushes and in their river at a cost every family can afford added reasons for eating crabs (Table 2).
Table 3 shows identi�ed cultural methods for preparing crab meal that contributed to reemergence of paragonimiasis in the study area.About 95% of the people eat uncooked crab with either alcohol, red pepper sauce, or with vinegar.Some 86% of the natives roasted or dried crabs and served it along African salad and Spinach made from oil bean seed and Amaranthus leaves, respectively.is delicacy is served mostly during traditional festivals.Generally 100% of people ground boiled crabs for short time as part of soup ingredients.
Table 4 shows that about 73% of the people did not wash ultensils (knife, mortar, and piston) used in preparing crab meal before using same ultensils in preparing other meals.is created great chances or possibilities of mechanical transporting metacercariae from one crab meal to other meals.
Table 5 shows that about 86.75% of people disposed excreta into river and near-by bushes around the homes, T 4: Habit towards washing of utensils aer crab meal preparation.

Habit
Number Percent Wash utensils aer crab meal preparation 108 27% Do not wash utensil aer crab meal preparation 292 73% Total 400 100% while sputum was generally disposed in the immediate environment/outside.is implied that a greater number of Paragonimus uterobilateralis eggs were constantly being discharged into the river and bushes where appropriate mollusces breed.e interactive discussions with the health workers showed that health workers at the health centers were not aware of paragonimiasis.Not even one paragonimiasis had been suspected or diagnosed in the health centers by the health workers, since that disease eradication exercise thirty years ago.Low index of suspicion of diagnosis of paragonimiasis had kept the reemergence unnoticed.All cases of cough and haemoptysis or rusty sputum had been investigated for a possible of pulmonary tuberculosis or HIV without the inclusion of paragonimiasis in the differential diagnosis.

Discussion
Evidence abounds of paragonimiasis reemergences in areas where it had been eradicated.In Japan, Maruyama et al. [11] and Nawa [12] have reported reemergence of paragonimiasis in areas where it was previously declared eradicated.In Nigeria, Enwereji and Eke [10] have also reported the reemergence of paragonimiasis.ere is a worrying indication of this disease spreading into areas following its reappearance.e reemergence elsewhere when it occurs shows that the circle of transmission of this disease is closed.e new move here is directed towards identifying the determinant factors including cultural norms of the people that contribute to the reemergence in order to plan a sustainable eradication programme.
e fact that the younger age group, 25 to 45 years, was less knowledgeable about paragonimiasis mode of transmission, prevention, and control than the older age group of 47 years and above shows that most of them had not been born at the time of the disease eradication in Nigeria.e few born at that time were about 6 years old and so were too young to comprehend and use the eradication lessons learnt at that time.e breakdown shows that the discontinuation of the preventive and control activities aer eradication contributed to the group being less apprehensive of paragonimiasis.e custom of eating crabs as a delicacy in Tables 2 and 3 created the avenue for disease reemergence.
Enwereji and Eke [10] argued that as long as the chain of transmission was broken and later became closed, the disease would certainly reemerge.Nawa [12] had earlier asserted that breaking circle of transmission only to close it up later caused reemergence of paragonimiasis in Japan.e unhygienic habit of not washing utensils properly aer preparing crab meals in of transmitting metacerariae from crabs to man.e present study identi�ed cultural practices of preparing and eating crabs raw and the unhygienic habit of not washing utensils used in preparing crab meal as contributing factors to the reemergence of paragonimiasis in Nigeria.is �nding is in keeping with the report of Lucas and Gilles [3] that infection can occur by eating uncooked crabs and cray�sh and also when encysted cercaria are le on the knife or other utensils used in preparing crab meal.e �nding that there was insanitary disposal of excreta and sputum into Imo River and nearby bushes could have contributed to reemergence of paragonimiasis in Nigeria, tallies with the report of some authors [3,8,13].ere is a need to note that the transmission of paragonimiasis is maintained by feacal and sputum pollution of water in which the appropriate snails and vectors crustaceans breed.
Lack of awareness of paragonimiasis amongst the health workers at the health centers caused the low level of index of suspicion amongst them.Awareness of the disease would have made the health workers continue to have high index of suspicion of the disease and then con�rm their suspicion by laboratory tests for cases of cough and haemoptysis which could have been caused by pulmonary paragonimiasis, in addition to pulmonary tuberculosis or HIV.
According to Shim et al. [14] variable paragonimiasis egg excretion of many patients can present negative stool result.erefore negative test for paragonimiasis could be mistaken for tuberculosis or other diseases.

Recommendation
is study was undertaken to highlight the need for surveillance and to ensure that there is no reemergence.Based on the �ndings in this study, we recommend the following.
(1) e health authorities and the policy makers should be health educated on how to check a reemergence.is training will enable them to know what they are expected to do to achieve success of the programme.
(2) Health information of the disease should be done on regular basis and involve all people at village and community levels.
(3) Routine disease surveillances system and noti�cation should be established to function as if they were put in place during the eradication programmes.
(4) Diagnostic and treatment facilities' workers should be given periodic lectures, seminars, and workshops on the disease information.
(5) New diagnostic and treatment procedures like Antigen detection assay indenti�eld by [15] should be established by the relevant authorities to facilitate the disease diagnosis.
(6) People should be health educated on the consequences of eating partally cooked or uncooked crabs as delicacies.erefore where crabs are the main source of protein intake, alternative but available and affordable protein substitute should be introduced.
With proper education on eradication of disease in place, effective and efficient surveillances program will be cost effective.
Table 4 also created another chance T 5: Cultural habit of disposing excreta and sputum (  ).