INTRODUCTION
Malaria, one of the most devastating human parasitic diseases, is prevalent in tropical developing regions, caus- ing great morbidity and mortality. Despite all control ef- forts, 3.4 billion people are still at risk of malaria, and approximately 207 million cases of malaria occur glo- bally each year1.
It is well known that human malaria is transmitted exclusively by anopheline mosquitoes. The susceptibility of Anopheles spp. to different human malarial parasites has been widely investigated. In 1929, Hindle and Feng2 studied the artificial infection rate of An. sinensis with the local Plasmodium vivax. Subsequently, more studies were undertaken to observe the development of P. vivax in An.
sinensis3–17. However, other culicine mosquito species, such as Aedes spp, Culex spp, and Mansonia spp, are also
abundantly present in malaria-endemic areas. Similar to the anophelines that feed on humans, culicines are impor- tant vectors for human disease, transmitting arboviruses and filarial worms. Although culicine mosquitoes have never been shown to transmit human malaria, they can transmit avian Plasmodium species to birds; and several studies18–20 have investigated whether different human- infectious Plasmodium spp. can complete their develop- ment in culicine mosquitoes. Depending on the mosquito and parasite species used, partial or complete develop- ment of Plasmodium has been observed in culicine mos- quitoes18–24. In 1937, Williamson and Zain21 infected Culex bitaeniorhyncus with P. falciparum, P. vivax and P.
malariae successfully, representing the first observation of human malarial parasites in a culicine mosquito. Oo- cysts have been observed in the midgut epithelium in Mansonia uniformis infected with P. falciparum25. Simi- Research Articles
A reassessment of the artificial infection of three predominant mosquito species with Plasmodium vivax in Shandong Province, China
Chongxing Zhang
1-2, Guihong Shi
1, Peng Cheng
1, Haifang Wang
1, Hongmei Liu
1, Lijuan Liu
1, Xiuxia Guo
1, Maoqing Gong
1, Yong Huang
11Department of Medical Entomology, Vector Biology Key Laboratory of Medicine and Health Shandong Province, Shandong Institute of Parasitic Diseases, Shandong Academy of Medical Sciences, Jining; 2Department of Collaborative Innovation Center for the Origin and Control of Emerging Infectious Diseases, Taishan Medical University, Taian, Shandong, China
ABSTRACT
Background & objectives: Under certain ecological circumstances, pathogens are able to rapidly adapt to new vectors. The great capacity of Plasmodium spp. to adapt to new anopheline mosquito vectors on different continents and the continuous ecological changes attributed to humans might promote their adaptation to culicine vectors, which are known to infect humans. Based on our current knowledge, it is difficult to predict whether such adaptations will occur. This study was aimed to determine the infection susceptibility of Anopheles sinensis, Culex tritaeniorhynchus and Cx. pipiens pallens to Plasmodium vivax in Shandong Province of China.
Methods: The susceptibility of the three predominant species of mosquitoes —An. sinensis, Cx. tritaeniorhynchus and Cx. pipiens pallens in Shandong Province was compared with a direct membrane feeding assay with 15 batches of Shandong strain mono-infected gametocyte-containing blood collected from Plasmodium vivax-infected patients. Infectivity was measured by dissecting the midguts and salivary glands of the mosquitoes. The presence of oocysts and sporozoites was determined by microscopy at 6 and 22 days post-blood feeding.
Results: From the 15 batches of mosquitoes that were fed infected blood, oocysts and sporozoites were detected only in 7th, 13th and 15th batches of infection for An. sinensis, and no oocysts or sporozoites were detected in Cx.
tritaeniorhynchus or Cx. pipiens pallens. The positive rate of An. sinensis infection was 21.2, 13 and 36.3% in the three batches of mosquitoes, with an average infection rate of 23.5%.
Interpretation & conclusion: The susceptibility of An. sinensis to P. vivax was very high in Shandong Province.
Cx. tritaeniorhynchus and Cx. pipiens pallens failed to exhibit susceptibility to P. vivax.
Key words Anopheles sinensis; Culex pipiens pallens; Culex tritaeniorhynchus; membrane blood feeding; Plasmodium vivax
larly, ookinetes have been observed in the blood meals of mosquitoes infected with Cx. salinarius23 and Cx.
quinquefasciatus26. Although, Alavi et al24 observed P.
berghei ookinetes in the blood meals of experimental Ae.
aegypti, the transmission experiment was unsuccessful.
Under certain ecological circumstances, pathogens are able to rapidly adapt to new vectors. For example, the chikungunya virus (CHIKV) was originally transmitted by Ae. aegypti. A single point mutation resulting in an amino acid replacement significantly increased the trans- mission efficiency of the virus in Ae. albopictus27. Plas- modium vivax adaptation to different anophelines in Mexico is also a very good example; in coastal areas, the parasites are transmitted by An. albimanus, the most com- mon anopheline in these areas, whereas at higher alti- tudes, the main vector is An. pseudopunctipennis, a foot- hill mosquito28–29. These examples show that pathogens, including Plasmodium spp, are able to adapt to new vec- tors rapidly following environmental changes30.
Due to the great capacity of Plasmodium spp. to adapt to new vectors on different continents, ongoing ecologi- cal changes caused by humans might promote the adap- tation of human-infectious Plasmodium parasites to culi- cines. The transmission of avian Plasmodium spp. by anopheline and culicine mosquitoes clearly suggests that such transmission might be possible for mammalian-in- fectious Plasmodium parasites. Based on our current knowledge, it is difficult to predict whether such adapta- tions will occur, and more research is needed to provide a more reliable prediction30.
In China, An. sinensis Wiedemann plays a major role in the maintenance of P. vivax malaria transmission31. Culex tritaeniorhynchus Giles is the primary vector of Japanese encephalitis (JE) virus, and Cx. pipiens pallens Coquillett is the primary vector of JE virus and filariasis in China32–33. Anopheles sinensis Wiedemann, Cx. pipiens pallens Coquillett and Cx. tritaeniorhynchus Giles (Diptera: Culicidae) are three dominant species in Shandong Province34. However, data on the susceptibil- ity of these three mosquitoes to P. vivax are rare in Shandong Province, and Cx. tritaeniorhynchus and Cx.
pipiens pallens have never been observed to be infected with P. vivax in China. The aim of this study was to in- vestigate the susceptibility and development of P. vivax in the three main species of mosquitoes in Shandong Prov- ince, China.
MATERIAL & METHODS Colonization of mosquitoes
This study was carried out in Jining, Shandong Prov-
ince, China from July to October 2010 and three mos- quito species—An. sinensis, Cx. tritaeniorhynchus and Cx. pipiens pallens were maintained in the laboratory of the Shandong Institute of Parasitic Diseases, Jining. These mosquitoes were reared using the methods described by Park et al35 in an insectary room at 27 ± 1°C and at 70- 80% relative humidity in a 12 h light/12 h dark cycle, and adult mosquitoes were raised with 10% (w/v) glucose with a sponge. For two days prior to blood feeding, the 6- to 8- day-old mosquitoes were provided only water.
Selection and screening of gametocyte patients
The only malaria parasite reported in the study area is Plasmodium vivax36. The patients who sought clinical treatment in Shandong Institute of Parasitic Diseases were screened for malarial parasites by a standard finger prick and Giemsa-stained blood smear. The patients who pre- sented with a high density of P. vivax in the blood (48–
385 P. vivax/100 leucocytes) and with an appropriate ga- metocyte count (0.5–30/100 P. vivax), as observed in a thin blood smear under a microscope, were selected. The screening took place the same day as the experimental infection of mosquitoes. A total of 1.5–2 ml of venous blood from the selected patients was drawn into heparin- ized tubes for the experimental feedings.
Experimental infections
Prior to the infectious blood meal, mosquitoes were starved for 1–2 days in the mosquito cages. Freshly drawn blood was immediately transferred to artificial membrane feeders that had been prewarmed to 37°C, as described previously16, 37–38. Finally, a fresh, washed amniotic mem- brane was tightly placed on the bowl and allowed to dry in the shade. Before the experiment, the dry amniotic membranes were prepared by moistening them with physi- ological saline and stretching them across the bottom of a 250 ml wide-mouth bottle, ensuring a proper gap between the amnion and the bottom, and using a rubber stopper with two glass tubes to plug the bottle mouth. During blood feeding, a constant-temperature (37°C) circulating- water system was used to prevent exflagellation of the microgametocytes39. Mosquitoes were allowed to feed for 20 min to 2 h each time. After being blood fed, all the engorged mosquitoes were reared for 10 days, and the stomach and the salivary glands of each mosquito were dissected under the microscope and checked for the pres- ence of oocysts and sporozoites.
Temperature and humidity indoors
The temperature and humidity were measured and recorded twice daily (800 and 1700 hrs) in the insectary
during the study period. The average temperature was 16.8–30°C, and the relative humidity was 70–98%. From blood feed to dissection, the average temperature was 20.3–
28.8°C in the insectary for 15 batches of mosquitoes.
Ethical approval
All human-subject research conducted in this study was reviewed and approved by the Institutional Ethics Committee of the Shandong Institute of Parasitic Diseases (SIPD), Shandong Academy of Medical Sciences. All the patients involved in this study read and signed informed consent forms.
RESULTS Patient data
More than 400 symptomatic malaria patients visited the Shandong Institute of Parasitic Diseases in Shandong during the study period. After screening, 185 volunteers were enrolled for the present study.
Percentage of positive mosquitoes
For An. sinensis, 195 mosquitoes were dissected among which 154 showed ovarian development and 41 were undeveloped (Tables 1 and 2), wheraeas 26 (13.3%) mosquitoes were positive for P. vivax; 11 (5.6%) were positive for oocysts; and 18 (9.2%) were positive for sporozoites. In the 154 mosquitoes with developed ova- ries, 10 (6.5%) were positive for stomach oocysts, 18 (11.6%) were positive for salivary gland sporozoites, three were positive for oocytes in the stomach and sporozoites in the salivary glands, and a total of 25 (16.2%) mosqui- toes were positive for stomach oocysts and salivary gland sporozoites. Only 1 of 41 (2.4%) of the ovarian- immature An. sinensis mosquitoes had an oocyst in the stomach, but sporozoites were not found in the salivary glands.
For Cx. tritaeniorhynchus, 203 mosquitoes were dissected (149 showed ovarian development, 54 were undeveloped), and 19 Cx. pipiens pallens were dissected (15 showed ovarian development, four were undevel- oped). The oocysts and sporozoites were not found in the stomachs or salivary glands in either of these two species of mosquitoes.
In the 11th batch, one blood-fed Cx. bitaeniorhyncus mosquito with an undeveloped ovary, and no oocysts or sporozoites were detected. Cx bitaeniorhyncus, however, is not a predominant mosquito species and was not in- cluded in Tables 1 and 2.
Infection condition
(i) Of the 15 batches of infectious blood that were
Table 1. Artificial infection in three predominant mosquito species with Plasmodium vivax (mosquitoes with full ovarian development). BatchClinicalP. vivax/100Gametocytes/FeedingDaysTemperatureAn. sinensisCx. tritaeniorhynchusCx. pipiens attackleucocytes100 P. vivaxdateafter(°C)No.No. positiveNo.No. positiveNo.No. positive timesblooddissectedSalivaryStomachdissectedSalivaryStomachDissectedSalivaryStomach feeding glandglandgland 12/Tertian2300.918 Jul10–1427.2700–––––– 22/Tertian1407.118 Jul10–1327.7100100––– 31/Day3660.530 Jul1428.2–––1100––– 43/Day3856.51 Aug13–1528.45003400––– 52/Day2400.99 Aug13–1428.8100800100 62/Tertian3323.611 Aug1428.5300100––– 75/Day831919 Aug8–1327.24791400100 83/Tertian2001020 Aug1426.510011001100 95/Tertian2323029 Aug12–1424.21004400––– 102/Tertian1581231 Aug11–1623.96001200100 112/Tertian6611.14 Sep14–1523.9––––––––– 123/Tertian9614.27 Sep1224.6––––––––– 134/Tertian160414 Sep6–1323.523301500100 142/Tertian4816.619 Sep15–2221.52600600––– 154/Day3803.921 Sep6–2020.33369200––– Total1541810149001500 (–) Not detected.
fed to the An. sinensis, Cx. tritaeniorhynchus, Cx. pipiens pallens and Cx. bitaeniorhyncus species of mosquitoes, only the 7th, 13th, and 15th batches yielded positive re- sults. In the three batches, 125 An. sinensis (103 with ovarian development, 22 undeveloped), 60 Cx.
tritaeniorhynchus (21 with ovarian development, 39 un- developed); and five Cx. pipiens pallens (2 with ovarian development, three undeveloped) were fed to engorge- ment. The positive rates of infection with P. vivax in An.
sinensis mosquitoes were 21.2, 13 and 36.3% in the three batches of mosquitoes, respectively, with an average of 23.5%; (ii) For the three batches of blood that yielded positive mosquitoes, the experimental blood was taken from patients who experienced malarial attacks 4–5 times per day. Among the three blood batches, two had >15 gametocytes per 100 leukocytes and the remaining batch had six gametocytes. The gametocyte rates were 19, 4 and 3.9% for the 7th, 13th and 15th batches, respectively;
and (iii) The days and temperature required for the ap- pearance of sporozoites in the mosquito salivary gland were nine days at an average temperature of 28.2°C in mid- to late August, 12 days at an average temperature of 24°C in mid- to late September, and 17 days at an average temperature of 20.5°C in late September to early October. In this experimental study, the sporozoi- tes and oocysts were observed for last time on the 11October 2010 (Tables 1 and 2).
DISCUSSION
From mid-July to early October 2010, individuals from the three predominant species of mosquitoes in Shandong Province, China, i.e. 195 An. sinensis, 203 Cx.
tritaeniorhynchus and 19 Cx. pipiens pallens, were sub- jected to artificial infection with the human malarial para- site P. vivax via membrane feedings. For Cx.
tritaeniorhynchus and Cx. pipiens pallens mosquitoes, this is the first study to evaluate the potential for infection with P. vivax in China.
Total 15 batches of 417 mosquitoes were dissected in three months during 2010. Of these, 26 mosquitoes from three batches totaling 190 mosquitoes (125 An.
sinensis, 60 Cx. tritaeniorhynchus and 5 Cx. pipiens pallens) were vivax positive. The results of susceptibility of An. sinensis to P. vivax were also consistent with ear- lier experiments2–4, 7, 9. The results proved that the sus- ceptibility of An. sinensis to P. vivax in Shandong Prov- ince is still very high.
The three batches of blood that produced P. vivax-posi- tive mosquitoes were obtained from patients who had been attacked by clinical malaria 4–5 times per day, with two batches having >15 gametocytes/100 leukocytes and one batch with 6.4 gametocytes/100 leukocytes. The patient who donated blood for the 15th batch was treated with an eight-day regimen of chloroquine and primaquine twice daily. This finding suggests that, regular treatment of pa- tients infected with malaria parasite is very important to control the spread and prevalence of malaria effectively.
The mosquitoes with complete ovary development were engorged fully. Those that did not fully engorge, failed to do so because the temperature was too low, which affected body fat accumulation, or because the ovaries were not fully developed. For the 15th batch (blood feed- ing studied in late September, dissection in early Octo- ber), mosquitoes with undeveloped ovaries accounted for more than half of the number of blood-fed mosquitoes due to the lower room temperature (average 20.3°C).
Although, P. falciparum and other human-infectious Plasmodium spp. come closest to completing their devel- opmental cycle in culicine mosquitoes18, oocysts, as well as sporozoites, have been also reported in Mansonia uniformis19. In infections of Ma. uniformis with P.
Table 2. Number of mosquitoes with undeveloped ovaries after blood feeding
Batches An. sinensis Cx. tritaeniorhynchus Cx. pipiens
No. dissected No. positive No. dissected No. positive No. dissected No. positive
Stomach Salivary Stomach Salivary Stomach Salivary
gland gland gland
7 4 0 0 – – – – – –
11 13 0 0 6 0 0 – – –
12 1 0 0 6 0 0 – – –
13 3 0 0 10 0 0 3 0 0
14 5 0 0 3 0 0 1 0 0
15 15 1 0 29 0 0 – – –
Total 41 1 0 54 0 0 4 0 0
(–) Not detected.
falciparum, only oocysts were found in the midgut epithe- lium25. The ookinetes have been observed in the blood meal of mosquitoes in studies with Cx. salinarius23, Cx.
quinquefasciatus26 and Ae. aegypti24. The ookinetes num- ber of P. falciparum in the blood meals of Cx.
quinquefasciatus were nearly the same as in their natural vector, An. gambiae26. It remains unclear, however, whether the results were comparable because of the use of different genotypes for the parasite and the vector40–42.
In this study, the locally predominant Cx.
tritaeniorhynchus and Cx. pipiens pallens were not infected with P. vivax. The results are consistent with an earlier study on Cx. bitaeniorhyncus and P. falciparum, in which no oocysts were observed in the midgut epithelium43. The transmission experiment with P. berghei in Ae. aegypti was also unsuccessful24. In infections of Ma. uniformis with P.
falciparum, no mosquitoes were maintained long enough to determine whether sporozoites would develop in the oocysts and invade the salivary glands25. It is still difficult to determine whether P. vivax infects Cx. tritaeniorhynchus and Cx. pipiens pallens in nature. In nature, avian plasmo- dia develop in and are typically transmitted by culicine mos- quitoes—Culex and Aedes. However, some avian malarial parasites, for example, P. gallinaceum, have been observed of being transmitted by Anopheles quadrimaculatus44–46, An. stephensi, and An. gambiae24, 47–48 under laboratory conditions. In a study also, Plasmodium-refractory and a Plasmodium-susceptible line of An. gambiae were geneti- cally selected, conferring either refractoriness or suscepti- bility to P. cynomolgi and P. gallinaceum and to some P.
falciparum (human malaria parasite) lines47. Similarly, a highly Plasmodium-susceptible line of An. stephensi was selected, and within a few generations, this line showed over 85% infection prevalence in P. gallinaceum48. Another species of avian malarial parasite, P. relictum, has been successfully transmitted between birds by An.
quadrimaculatus, An. albimanus46, 49, An. crucians46, and An. freeborni46, 50.
These results demonstrate that the establishment of the parasite in new regions almost always depends on vector switches51–52. Nevertheless, human-infectious Plas- modium spp. have only adapted so far to different anopheline species and not to culicine mosquitoes. The ability of mammalian-infectious Plasmodium parasites to develop in culicine mosquitoes is highly dependent on the combination of the mosquito and parasite species used30.
CONCLUSION
The susceptibility of An. sinensis in Shandong Prov- ince to P. vivax appeared very high when evaluated with
membrane feeding assay under laboratory conditions.
Oocysts and sporozoites were detected only in three batches of mosquitoes for An. sinensis infection, out of the 15 batches that were fed infected blood. In these three batches, the positive rate of An. sinensis infection was 21.2, 13 and 36.3%, with an average infection rate of 23.5%. The other two predominant species of mosqui- toes, Cx. tritaeniorhynchus and Cx. pipiens pallens, failed to show susceptibility to P. vivax.
Conflict of interest
The authors declare that they have no any conflict of interest.
ACKNOWLEDGEMENTS
The project was sponsored by the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry under the Shandong Natural Science Foundation (Grant No. ZR2014YL038) and the Joint Research and Development Project of the Sino- Thai Scientific and Technical Cooperation (Grant No. 21- RD-05).
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Correspondence to: Mr. Yong Huang/Mr. Maoqing Gong, Department of Medical Entomology, Vector Biology Key Laboratory of Medicine and Health Shandong Province, Shandong Institute of Parasitic Diseases, Shandong Academy of Medical Sciences, Jining, Shandong 272033, People’s Republic of China.
E-mail: [email protected]; [email protected] Received: 13 May 2016 Accepted in revised form: 21 July 2016
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